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Health Economics Research in Primary Prevention of Cancer: Assessment, Current Challenges, and Future Directions

Health Economics Research in Primary Prevention of Cancer: Assessment, Current Challenges, and... Abstract In the past 2 decades, the demand for information on health economics research to guide health care decision making has substantially increased. Studies have provided evidence that eliminating or reducing tobacco use; eating a healthy diet, including fruit and vegetables; being physically active; reducing alcohol consumption; avoiding ultraviolet radiation; and minimizing exposure to environmental and occupational carcinogenic agents should substantially reduce cancer incidence in the population. The benefits of these primary prevention measures in reducing cancer incidence are not instantaneous. Therefore, health economics research has an important role to play in providing credible information to decision makers on the health and economic benefits of primary prevention. This article provides an overview of health economics research related to primary prevention of cancer. We addressed the following questions: 1) What are the gaps and unmet needs for performing health economics research focused on primary prevention of cancer? 2) What are the challenges and opportunities to conducting health economics research to evaluate primary prevention of cancer? and 3) What are the future directions for enhancing health economics research on primary prevention of cancer? Modeling primary prevention of cancer is often difficult given data limitations, long delays before the policy or intervention is effective, possible unintended effects of the policy or intervention, and the necessity of outside expertise to understand key inputs or outputs to the modeling. Despite these challenges, health economics research has an important role to play in providing credible information to decision makers on the health and economic benefits of primary prevention of cancer. In the past decades, the overall annual cancer death rates have continued to decline for all cancer sites combined (1), and the United States is making substantial progress in reducing cancer death rates, as evident in the meeting of Healthy People 2020 targets (2). However, changes in cancer incidence rates were mixed, with new cases leveling off in men and slightly increasing in women (1). Similarly, during the past 5 years, the overall cancer incidence rates in children 15 years and younger, adolescents, and young adults have increased (1). Cancer remains the second leading cause of death in the United States (3), with substantial negative outcomes to quality of life and life expectancy. In addition to the health burden, cancer also has substantial economic impacts on patients, their families, caregivers, employers, and the health-care system. For example, in a recent study, medical care costs for cancer in the United States were estimated to be $185 billion in 2015 and were projected to increase to more than $240 billion by 2030 based only on population growth (4). As a result, efforts to prevent new cases of cancer are paramount to substantially reducing cancer-related mortality. These efforts would likely benefit from concerted resources devoted to primary prevention, keeping people healthy and cancer free. In general, preventing health conditions such as cancer involves at least 3 broad categories: primary, secondary, and tertiary prevention (5). Primary prevention focuses on interventions to lower cancer risk so fewer cases of cancer ever occur. An example of such an intervention is the human papillomavirus (HPV) vaccination to prevent infection and the subsequent occurrence of HPV-associated cancers (cervical, oropharyngeal, vulva, vagina, penis, anus). Secondary prevention seeks to prevent the progression of cancer by focusing on interventions such as screening and early detection of cancer. An example of such an intervention is mammography for breast cancer screening. The final category is tertiary prevention, which aims to reduce death or severity of cancer in an individual through clinical interventions such as treatment and rehabilitation. This study focuses on primary prevention. This article is part of a collection of articles on “The Future of Cancer Health Economics Research,” a virtual conference sponsored and hosted by the National Cancer Institute (NCI) in December 2020. In this article, the Primary Prevention of Cancer Planning Group (Planning Group) was charged to focus on 1 aspect of the cancer control continuum: prevention (6). Other planning groups within the virtual conference focused on different areas of the cancer control continuum (ie, screening, treatment, and survivorship). Articles on these areas of the cancer control continuum are included in the collection (7-9). All planning groups were charged to address the following issues: 1) What are the gaps and unmet needs for performing health economics research focused on cancer? 2) What are the challenges and opportunities to conducting cancer health economics research? and 3) What are the future directions for enhancing health economics research to address these needs and support primary cancer prevention? In this article, we take a broad approach to our description of cancer health economics research. This includes 1) economic evaluations that provide evidence that guides how to allocate scarce resources most efficiently for cancer prevention, and 2) applied micro-econometric research that provides evidence about the causal relationships between specific cancer risk factors and outcomes. Methods Before the December 2020 virtual conference, the Primary Prevention of Cancer Planning Group convened several meetings from August to November 2020. The planning group consisted of health economists and health services researchers who are experts in cancer control, sexually transmitted infections, tobacco use, and other health conditions or behaviors related to primary prevention of cancer. Group members came from different organizational and institutional settings. To guide our deliberation and discussions, the planning group proposed a framework for the economics of primary prevention of cancer (Figure 1) to supplement the previously published framework on cancer health economics research (6). Figure 1. Open in new tabDownload slide Framework for conducting health economics research on primary prevention of cancer. *Stages of lifespan were adopted from the CDC’s Preventing Cancer Across a Lifetime initiative (10). Figure 1. Open in new tabDownload slide Framework for conducting health economics research on primary prevention of cancer. *Stages of lifespan were adopted from the CDC’s Preventing Cancer Across a Lifetime initiative (10). In the proposed framework, the planning group recognized that cancer is caused by a complex web of multiple factors that are multi-stage in nature (11). As such, it may be impossible to identify all the factors that could be addressed by primary prevention. However, the planning group identified 3 broad factors that encompass all aspects of cancer related to prevention: 1) genetic and biological, 2) environmental and occupational, and 3) behavioral. For each of these factors, several epidemiological and behavioral studies have reported evidence of interventions to reduce the incidence of cancer (12-16). Despite strong evidence for the effectiveness of prevention, gaps remain in health economics research on primary intervention to reduce cancer incidence. According to Harvey Fineberg, the former President of the National Academy of Medicine (formerly the Institute of Medicine), the gap exists because “Prevention is a hard sell” (17). He stated, “There is no drama in prevention; non‐events are not counted; statistical lives don’t have immediacy; […]; prevention often runs against commercial interests; it may conflict with personal preferences or religious beliefs; and there is declining trust in leaders and institutions challenging people’s willingness to follow guidelines” (17). These issues articulated by Feinberg are part of the case for the economics of primary prevention. For instance, in the past 30 years, only 7.1% of health economic studies in which the outcomes were measured in quality-adjusted life-years gained in cancer disease were conducted in primary prevention compared with 68.4% of studies conducted in tertiary prevention. In this article, first, we describe primary prevention of cancer. Second, we identify existing primary prevention interventions to prevent or reduce the incidence of cancer. Third, we describe the gaps and unmet needs for performing health economics research focused on primary prevention of cancer. Fourth, we address the challenges to conducting cancer health economics research. Fifth, we discuss the opportunities to conduct health economics research focused on primary prevention of cancer. Finally, we discuss future directions for enhancing and supporting primary prevention of cancer health economics research. Factors That Can Increase Cancer Risk Many factors can contribute to the risk of developing cancer over a lifetime. These may include foods and beverages we consume, chemicals and radiation we are exposed to, and viruses and bacteria we encounter (18). Cancer risk can be influenced by endogenous factors such as inherited genes, hormones, immunologic conditions, and other characteristics of individuals such as age and sex (19). Exogenous (environmental) factors affecting cancer risk may occur in occupational or home settings and involve socioeconomic status, behavioral factors, stress, and infectious agents (20). These factors interact with each other (Figure 1) and may include carcinogenic substances or effects that can damage one’s DNA, causing the initiation and progression of some cancers (21-23). The initiation and progression process can even start as early as prenatal and progress through all life stages to older adulthood (Figure 1) (24,25). For example, repeated occupational exposures to carcinogenic agents by an individual at childbearing age may increase the risk of cancer in their offspring (26). Some epidemiologists have estimated that from 30% to 50% of cancers are preventable (27–29), based on epidemiologic studies demonstrating a causal relationship with many exogenous factors (20). In addition, although age has been recognized as a nonmodifiable risk factor for cancer (30), a commentary cast doubt on the notion that cancer cannot be prevented among older adults (31). That is, age as a risk factor reflects the biology of aging as well as the cumulative effect of environmental and occupational exposures, chronic conditions (diabetes, obesity), and behavioral factors acquired during a lifetime, and these risk factors can potentially be prevented or modified. Although some cancers are associated with inherited genetic mutations (eg, certain breast and ovarian cancers, colorectal, and skin cancers), primary prevention interventions such as genetic counseling and testing can help reduce the incidence of these cancers (32,33). Some of the genes, their associated cancers, and recommended interventions are presented in Table 1. Table 1. Selected genes and infectious agents by risk factors associated with exposure, outcomes of the exposure, and primary intervention measuresa,b Exposure factors . Selected risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for the exposure . Reference . Selected genes associated with risk of each cancer Lynch syndrome (MLH1, MSH2, MSH6, PMS2, EPCAM) Colorectal cancer Chemoprevention (eg, aspirin and some vitamins), genetic counseling and genetic testing (32, 34) BRCA1 and BRCA2 Breast and ovarian cancer Genetic counseling and genetic testing, prophylactic mastectomy, chemoprevention (tamoxifen or raloxifene) (33) CDKN2A and CDK4 Malignant melanoma Protection from ultraviolet radiation, avoidance of recreational outdoor sunbathing, avoidance of tanning beds or tanning salons, prohibiting tanning bed access for minors (35) SCLC1 Lung cancer Abstinence from smoking, smoking cessation; avoidance of secondhand smoke (36) HPC1+, TLR variants Prostate cancer Chemoprevention with finasteride, dutasteride; choosing a low-fat diet (37) DPC4 Pancreatic cancerc Suggested prevention: adherence to preventive behavioral factors discussed in this article (11) Selected infectious agents HBV HCC/liver cancer Vaccination with prophylactic HBV vaccine (38) HCV HCC/liver cancer Testing and treatment with antiviral drugs (39) HPV-6, 11, 16, and 18 Cervical, vulvar, vaginal, and anal cancers and dysplasia; genital warts Vaccination with prophylactic quadrivalent HPV vaccine (40) HPV 16, 18, 31, 33, 45, 52, and 58 Cervical, oropharyngeal vulvar, vaginal, and anal cancers and dysplasia Vaccination with prophylactic 9-valent HPV vaccine (41, 42) Helicobacter pylori Gastric cancers Testing and treating with a combination of stomach acid suppressants and antibiotics (43) HIV Lymphoma; Kaposi sarcoma Testing and treating with a combination of antiviral drugs (44) Exposure factors . Selected risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for the exposure . Reference . Selected genes associated with risk of each cancer Lynch syndrome (MLH1, MSH2, MSH6, PMS2, EPCAM) Colorectal cancer Chemoprevention (eg, aspirin and some vitamins), genetic counseling and genetic testing (32, 34) BRCA1 and BRCA2 Breast and ovarian cancer Genetic counseling and genetic testing, prophylactic mastectomy, chemoprevention (tamoxifen or raloxifene) (33) CDKN2A and CDK4 Malignant melanoma Protection from ultraviolet radiation, avoidance of recreational outdoor sunbathing, avoidance of tanning beds or tanning salons, prohibiting tanning bed access for minors (35) SCLC1 Lung cancer Abstinence from smoking, smoking cessation; avoidance of secondhand smoke (36) HPC1+, TLR variants Prostate cancer Chemoprevention with finasteride, dutasteride; choosing a low-fat diet (37) DPC4 Pancreatic cancerc Suggested prevention: adherence to preventive behavioral factors discussed in this article (11) Selected infectious agents HBV HCC/liver cancer Vaccination with prophylactic HBV vaccine (38) HCV HCC/liver cancer Testing and treatment with antiviral drugs (39) HPV-6, 11, 16, and 18 Cervical, vulvar, vaginal, and anal cancers and dysplasia; genital warts Vaccination with prophylactic quadrivalent HPV vaccine (40) HPV 16, 18, 31, 33, 45, 52, and 58 Cervical, oropharyngeal vulvar, vaginal, and anal cancers and dysplasia Vaccination with prophylactic 9-valent HPV vaccine (41, 42) Helicobacter pylori Gastric cancers Testing and treating with a combination of stomach acid suppressants and antibiotics (43) HIV Lymphoma; Kaposi sarcoma Testing and treating with a combination of antiviral drugs (44) a Source: authors’ compilation. HBV = hepatitis B virus; HCC = hepatocellular carcinoma; HCV = hepatitis C virus; HPC1 = hereditary prostate cancer 1; HPV = human papilloma virus; TLR = toll-like receptor. b This table provides additional details on 1 of the exposure factors (genetics or biological) presented in Figure 1. In addition, the potential primary intervention measures included in the table can be quantified through health economics research. c Available evidence suggests that lifestyle and behavioral modifications and limiting exposure to certain chemicals in the workplace can reduce the risk of pancreatic cancer. Open in new tab Table 1. Selected genes and infectious agents by risk factors associated with exposure, outcomes of the exposure, and primary intervention measuresa,b Exposure factors . Selected risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for the exposure . Reference . Selected genes associated with risk of each cancer Lynch syndrome (MLH1, MSH2, MSH6, PMS2, EPCAM) Colorectal cancer Chemoprevention (eg, aspirin and some vitamins), genetic counseling and genetic testing (32, 34) BRCA1 and BRCA2 Breast and ovarian cancer Genetic counseling and genetic testing, prophylactic mastectomy, chemoprevention (tamoxifen or raloxifene) (33) CDKN2A and CDK4 Malignant melanoma Protection from ultraviolet radiation, avoidance of recreational outdoor sunbathing, avoidance of tanning beds or tanning salons, prohibiting tanning bed access for minors (35) SCLC1 Lung cancer Abstinence from smoking, smoking cessation; avoidance of secondhand smoke (36) HPC1+, TLR variants Prostate cancer Chemoprevention with finasteride, dutasteride; choosing a low-fat diet (37) DPC4 Pancreatic cancerc Suggested prevention: adherence to preventive behavioral factors discussed in this article (11) Selected infectious agents HBV HCC/liver cancer Vaccination with prophylactic HBV vaccine (38) HCV HCC/liver cancer Testing and treatment with antiviral drugs (39) HPV-6, 11, 16, and 18 Cervical, vulvar, vaginal, and anal cancers and dysplasia; genital warts Vaccination with prophylactic quadrivalent HPV vaccine (40) HPV 16, 18, 31, 33, 45, 52, and 58 Cervical, oropharyngeal vulvar, vaginal, and anal cancers and dysplasia Vaccination with prophylactic 9-valent HPV vaccine (41, 42) Helicobacter pylori Gastric cancers Testing and treating with a combination of stomach acid suppressants and antibiotics (43) HIV Lymphoma; Kaposi sarcoma Testing and treating with a combination of antiviral drugs (44) Exposure factors . Selected risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for the exposure . Reference . Selected genes associated with risk of each cancer Lynch syndrome (MLH1, MSH2, MSH6, PMS2, EPCAM) Colorectal cancer Chemoprevention (eg, aspirin and some vitamins), genetic counseling and genetic testing (32, 34) BRCA1 and BRCA2 Breast and ovarian cancer Genetic counseling and genetic testing, prophylactic mastectomy, chemoprevention (tamoxifen or raloxifene) (33) CDKN2A and CDK4 Malignant melanoma Protection from ultraviolet radiation, avoidance of recreational outdoor sunbathing, avoidance of tanning beds or tanning salons, prohibiting tanning bed access for minors (35) SCLC1 Lung cancer Abstinence from smoking, smoking cessation; avoidance of secondhand smoke (36) HPC1+, TLR variants Prostate cancer Chemoprevention with finasteride, dutasteride; choosing a low-fat diet (37) DPC4 Pancreatic cancerc Suggested prevention: adherence to preventive behavioral factors discussed in this article (11) Selected infectious agents HBV HCC/liver cancer Vaccination with prophylactic HBV vaccine (38) HCV HCC/liver cancer Testing and treatment with antiviral drugs (39) HPV-6, 11, 16, and 18 Cervical, vulvar, vaginal, and anal cancers and dysplasia; genital warts Vaccination with prophylactic quadrivalent HPV vaccine (40) HPV 16, 18, 31, 33, 45, 52, and 58 Cervical, oropharyngeal vulvar, vaginal, and anal cancers and dysplasia Vaccination with prophylactic 9-valent HPV vaccine (41, 42) Helicobacter pylori Gastric cancers Testing and treating with a combination of stomach acid suppressants and antibiotics (43) HIV Lymphoma; Kaposi sarcoma Testing and treating with a combination of antiviral drugs (44) a Source: authors’ compilation. HBV = hepatitis B virus; HCC = hepatocellular carcinoma; HCV = hepatitis C virus; HPC1 = hereditary prostate cancer 1; HPV = human papilloma virus; TLR = toll-like receptor. b This table provides additional details on 1 of the exposure factors (genetics or biological) presented in Figure 1. In addition, the potential primary intervention measures included in the table can be quantified through health economics research. c Available evidence suggests that lifestyle and behavioral modifications and limiting exposure to certain chemicals in the workplace can reduce the risk of pancreatic cancer. Open in new tab Certain viruses, bacteria, and parasites are 1 source of cancer initiation in humans. Overall, it has been estimated that infectious agents represent 15% to 20% of all cancers in humans (45,46). The International Agency for Research on Cancer has classified at least 11 infectious pathogens as human carcinogens (47). These cancer-causing pathogens include HPV, hepatitis B virus, hepatitis C virus, Epstein-Barr virus, HIV-1, Helicobacter pylori, opisthorchis viverrine, and other agents (38-41,43,44,48). Some of these viruses, their associated cancers, and recommended primary intervention measures are presented in Table 1. These intervention measures can be quantified through health economics research, and the outcomes can help to inform policy decisions. Environmental and Occupational Exposures Environment and occupation are another major exposure factor to cancer-causing carcinogenic substances. The availability of evidence to evaluate the association of specific environmental and occupational exposures and various cancers is very limited, and testing for most chemicals is still incomplete. The International Agency for Research on Cancer and the National Toxicology Program have classified many carcinogenic substances as “sufficient evidence,” indicating a causal relation between exposure to the agent and human cancer, and as “limited evidence,” defined as the observation of a (noncausal) positive association between exposure to the agent and human cancer (49–51). These carcinogenic agents (both sufficient and limited evidence) include specific outdoor and indoor air pollutants, nitrates, pesticides, dioxins, environmental tobacco smoke, certain food additives, benzene, asbestos, solvents, fibers, fine-particle dust (eg, PM2.5), metals, radiation (ionizing and nonionizing), and many other agents. Exposure to these agents may occur on multiple occasions and in various settings during a lifetime, including at workplaces, homes, schools, and entertainment venues. Some of the types of cancers induced by these carcinogens are presented in Table 2. The contributions of these carcinogenic agents to cancer in the United States are substantial. For example, a recent World Health Organization study reported a general estimate that approximately 20% of all cancers are associated with environmental factors and 2% to 10% are associated with occupational exposure (68). These estimates highlight the importance of continued efforts to implement evidence-based primary prevention interventions to prevent these exposures, and health economics research helps to quantify the burden associated with these exposures to inform health policy decisions. Table 2. Selected environmental and occupational carcinogens by risk factors associated with exposure, outcomes, and primary intervention measuresa Exposure factors . Selected risk factors associated with exposureb . Selected outcomes of exposurec . Selected potential primary intervention measures for the exposured . Reference . Environmental carcinogens Nitrates in drinking water Leukemia, bladder, lymphoma, and colorectal cancer Use treatment processes such as installation of ion exchange resin; distillation; reverse osmosis system (52) Motor vehicle exhaust (nitrogen dioxide) Childhood leukemia, central nervous system cancers Reduce outdoor air pollution from motor vehicle traffic by improving infrastructure that supports public transportation, bikeable roads, and other alternatives; use traffic controls that reduce congestion and idling; improve measures to reduce the number of vehicles on the road, such as telecommuting, flexible work hours, and rideshares, and commuting by bicycle (14, 42, 53–55) Indoor air pollutantsb Childhood leukemia and lymphoma cancers Ban of smoking cigarettes in indoor workplaces, public transportation, and indoor public places; reduce burning of wood, incense, or candles and use of gas cooking and heating appliances; reduce workers’ exposure to contaminated air at smokehouses, trash incineration facilities, oil refinery plants, and coal tar and asphalt production plants (53, 56, 57) Environmental organic pollutants (in utero) or POPs Testicular cancer Regulate carcinogenic chemicals such as exposure to pesticides; minimize exposure to POPs through ingestion and inhalation; encourage people of reproductive age to avoid eating large fish, fatty meat, and dairy products that have relatively high levels of POPs and to increase consumption of fibrous foods and green vegetables such as spinach and kale (23, 58) Pesticides such as dioxins Childhood leukemia and lymphoma, brain tumors, germ cell tumors, Hodgkin, NHL Reduce use of pesticides in residential lawns and gardens; reduce direct exposure to pesticides by children; reduce use of pesticides in agricultural products, foods, and drinking water (21, 53) PAHs Lung cancer Encourage people to reduce consumption of smoked and charbroiled foods; avoid exposure to dust, fumes, and skin contact by wearing protective clothing, such as long-sleeve shirts, long pants, and gloves when working with products containing PAHs; eliminate exposure to tobacco smoke; avoid cooking food at very high temperatures and avoid contact of foods with open flames (22) Nitrate consumption Bladder cancer Encourage people to minimize consumption of processed foods and limit meat products such as hot dogs and sausage; eat organic food; eat a diet high in antioxidants (59) Occupational exposures Asbestos Laryngeal, lung, mesothelioma Prohibit use of asbestos in the home and at work; ban export of asbestos; provide asbestos awareness training; provide medical surveillance to workers exposed to asbestos (11, 21) Wood dust Lung, nasal and nasopharynx Encourage or require that workers/supervisors install exhaust ventilation system with collectors placed at points where dust is produced; provide personal protective equipment to reduce wood dust exposure; require wearing of respirators to remove hazardous particulates (dusts) (60) Petroleum products, motor vehicle exhaust (eg, diesel, PAHs, soot, and dioxins) Lung, NHL, soft-tissue sarcoma, skin Increase use of renewable products; perform thermal treatment of waste and clean coal technologies; minimize children’s exposure to toxins (11, 21) Metals (arsenic) Bladder, lung, skin, soft-tissue sarcoma of the liver Reduce exposure to arsenic in food and in safe drinking water and air (53) Reactive chemicals (vinyl chloride) Liver and biliary, soft-tissue sarcoma (angiosarcoma of the liver) Limit chronic or long-term exposure to vinyl chloride; limit use of polyvinyl chloride plastic containers and food packaging; encourage industrial workers in close contact with vinyl chloride to use respirators and wear protective clothing; avoid tobacco smoke (61, 62) Solvents (benzene) Leukemia, NHL Ensure that workers know that if benzene was released indoors, they should go out of the building; if outdoors, should leave the area and move to an area with fresh air; if exposed to benzene, should remove and dispose their clothes, rapidly wash their entire body with soap and water, and get medical care as quickly as possible; practice use of effective personal protective equipment such as breathing protection, helmet with fresh air supply, and face covering operating with positive pressure to blow clean air from inside helmet (47, 63–65) Radiation (ionizing) Bone, brain and central nervous system, breast, leukemia, liver and biliary, lung, multiple myeloma, soft-tissue sarcoma, skin, thyroid Design public policies to avoid unnecessary exposure, including legislation to promote appropriate use of radiological medical procedures; educate physicians to promote use of referral guidelines as decision-making tools to justify diagnostic procedures of choice; educate and train imaging professionals (radiologists and technicians) to apply diagnostic reference levels to radiological procedures to reduce radiation doses without affecting image quality; “Image Wisely”e—encourages imaging providers to limit medical radiation (eg, CT scan, X-rays) in adults; “Image Gently”—elimination of unnecessary testing to minimize radiation in children (63, 66, 67) Radiation (ultraviolet) Skin cancer (basal cell and squamous cell carcinomas) and malignant melanoma Reduce exposure to sun and increase provision of shade in public areas, especially for children and adolescents; encourage people to increase use of sunscreen and avoid using tanning lamps or beds (16, 35) Exposure factors . Selected risk factors associated with exposureb . Selected outcomes of exposurec . Selected potential primary intervention measures for the exposured . Reference . Environmental carcinogens Nitrates in drinking water Leukemia, bladder, lymphoma, and colorectal cancer Use treatment processes such as installation of ion exchange resin; distillation; reverse osmosis system (52) Motor vehicle exhaust (nitrogen dioxide) Childhood leukemia, central nervous system cancers Reduce outdoor air pollution from motor vehicle traffic by improving infrastructure that supports public transportation, bikeable roads, and other alternatives; use traffic controls that reduce congestion and idling; improve measures to reduce the number of vehicles on the road, such as telecommuting, flexible work hours, and rideshares, and commuting by bicycle (14, 42, 53–55) Indoor air pollutantsb Childhood leukemia and lymphoma cancers Ban of smoking cigarettes in indoor workplaces, public transportation, and indoor public places; reduce burning of wood, incense, or candles and use of gas cooking and heating appliances; reduce workers’ exposure to contaminated air at smokehouses, trash incineration facilities, oil refinery plants, and coal tar and asphalt production plants (53, 56, 57) Environmental organic pollutants (in utero) or POPs Testicular cancer Regulate carcinogenic chemicals such as exposure to pesticides; minimize exposure to POPs through ingestion and inhalation; encourage people of reproductive age to avoid eating large fish, fatty meat, and dairy products that have relatively high levels of POPs and to increase consumption of fibrous foods and green vegetables such as spinach and kale (23, 58) Pesticides such as dioxins Childhood leukemia and lymphoma, brain tumors, germ cell tumors, Hodgkin, NHL Reduce use of pesticides in residential lawns and gardens; reduce direct exposure to pesticides by children; reduce use of pesticides in agricultural products, foods, and drinking water (21, 53) PAHs Lung cancer Encourage people to reduce consumption of smoked and charbroiled foods; avoid exposure to dust, fumes, and skin contact by wearing protective clothing, such as long-sleeve shirts, long pants, and gloves when working with products containing PAHs; eliminate exposure to tobacco smoke; avoid cooking food at very high temperatures and avoid contact of foods with open flames (22) Nitrate consumption Bladder cancer Encourage people to minimize consumption of processed foods and limit meat products such as hot dogs and sausage; eat organic food; eat a diet high in antioxidants (59) Occupational exposures Asbestos Laryngeal, lung, mesothelioma Prohibit use of asbestos in the home and at work; ban export of asbestos; provide asbestos awareness training; provide medical surveillance to workers exposed to asbestos (11, 21) Wood dust Lung, nasal and nasopharynx Encourage or require that workers/supervisors install exhaust ventilation system with collectors placed at points where dust is produced; provide personal protective equipment to reduce wood dust exposure; require wearing of respirators to remove hazardous particulates (dusts) (60) Petroleum products, motor vehicle exhaust (eg, diesel, PAHs, soot, and dioxins) Lung, NHL, soft-tissue sarcoma, skin Increase use of renewable products; perform thermal treatment of waste and clean coal technologies; minimize children’s exposure to toxins (11, 21) Metals (arsenic) Bladder, lung, skin, soft-tissue sarcoma of the liver Reduce exposure to arsenic in food and in safe drinking water and air (53) Reactive chemicals (vinyl chloride) Liver and biliary, soft-tissue sarcoma (angiosarcoma of the liver) Limit chronic or long-term exposure to vinyl chloride; limit use of polyvinyl chloride plastic containers and food packaging; encourage industrial workers in close contact with vinyl chloride to use respirators and wear protective clothing; avoid tobacco smoke (61, 62) Solvents (benzene) Leukemia, NHL Ensure that workers know that if benzene was released indoors, they should go out of the building; if outdoors, should leave the area and move to an area with fresh air; if exposed to benzene, should remove and dispose their clothes, rapidly wash their entire body with soap and water, and get medical care as quickly as possible; practice use of effective personal protective equipment such as breathing protection, helmet with fresh air supply, and face covering operating with positive pressure to blow clean air from inside helmet (47, 63–65) Radiation (ionizing) Bone, brain and central nervous system, breast, leukemia, liver and biliary, lung, multiple myeloma, soft-tissue sarcoma, skin, thyroid Design public policies to avoid unnecessary exposure, including legislation to promote appropriate use of radiological medical procedures; educate physicians to promote use of referral guidelines as decision-making tools to justify diagnostic procedures of choice; educate and train imaging professionals (radiologists and technicians) to apply diagnostic reference levels to radiological procedures to reduce radiation doses without affecting image quality; “Image Wisely”e—encourages imaging providers to limit medical radiation (eg, CT scan, X-rays) in adults; “Image Gently”—elimination of unnecessary testing to minimize radiation in children (63, 66, 67) Radiation (ultraviolet) Skin cancer (basal cell and squamous cell carcinomas) and malignant melanoma Reduce exposure to sun and increase provision of shade in public areas, especially for children and adolescents; encourage people to increase use of sunscreen and avoid using tanning lamps or beds (16, 35) a Source: authors’ compilation. This table provided more details on one of the exposure factors (environmental and occupational) presented in the figure. NHL = non-Hodgkin’s lymphoma; PAH = poly-aromatic hydrocarbon; POP = persistent organic pollutant. b Selected risk factors associated with exposure (carcinogenic agent) based on a Group 1 designation by the International Agency for Research on Cancer (44, 49, 50). c Selected outcomes of the exposure are those classified as “strong evidence” of causal link to the carcinogenic agent based on a Group 1 designation by the International Agency for Research on Cancer (44, 49, 50). d The effectiveness and economic impact of some of these environmental and occupational primary prevention measures have not been quantified. This is partly due to lack of data. With data, health economics research can help quantify their economic benefits. e Image Wisely encourages imaging providers to 1) optimize use of radiation to use only the radiation necessary to produce diagnostic quality images; 2) convey the principles of the Image Wisely initiative to the imaging team to ensure that the facility optimizes its use of radiation when imaging patients; 3) communicate optimal patient imaging strategies to referring physicians and be available for consultation; and 4) routinely review imaging protocols to ensure the use of the least amount of radiation necessary to acquire a quality diagnostic image (63, 67). Open in new tab Table 2. Selected environmental and occupational carcinogens by risk factors associated with exposure, outcomes, and primary intervention measuresa Exposure factors . Selected risk factors associated with exposureb . Selected outcomes of exposurec . Selected potential primary intervention measures for the exposured . Reference . Environmental carcinogens Nitrates in drinking water Leukemia, bladder, lymphoma, and colorectal cancer Use treatment processes such as installation of ion exchange resin; distillation; reverse osmosis system (52) Motor vehicle exhaust (nitrogen dioxide) Childhood leukemia, central nervous system cancers Reduce outdoor air pollution from motor vehicle traffic by improving infrastructure that supports public transportation, bikeable roads, and other alternatives; use traffic controls that reduce congestion and idling; improve measures to reduce the number of vehicles on the road, such as telecommuting, flexible work hours, and rideshares, and commuting by bicycle (14, 42, 53–55) Indoor air pollutantsb Childhood leukemia and lymphoma cancers Ban of smoking cigarettes in indoor workplaces, public transportation, and indoor public places; reduce burning of wood, incense, or candles and use of gas cooking and heating appliances; reduce workers’ exposure to contaminated air at smokehouses, trash incineration facilities, oil refinery plants, and coal tar and asphalt production plants (53, 56, 57) Environmental organic pollutants (in utero) or POPs Testicular cancer Regulate carcinogenic chemicals such as exposure to pesticides; minimize exposure to POPs through ingestion and inhalation; encourage people of reproductive age to avoid eating large fish, fatty meat, and dairy products that have relatively high levels of POPs and to increase consumption of fibrous foods and green vegetables such as spinach and kale (23, 58) Pesticides such as dioxins Childhood leukemia and lymphoma, brain tumors, germ cell tumors, Hodgkin, NHL Reduce use of pesticides in residential lawns and gardens; reduce direct exposure to pesticides by children; reduce use of pesticides in agricultural products, foods, and drinking water (21, 53) PAHs Lung cancer Encourage people to reduce consumption of smoked and charbroiled foods; avoid exposure to dust, fumes, and skin contact by wearing protective clothing, such as long-sleeve shirts, long pants, and gloves when working with products containing PAHs; eliminate exposure to tobacco smoke; avoid cooking food at very high temperatures and avoid contact of foods with open flames (22) Nitrate consumption Bladder cancer Encourage people to minimize consumption of processed foods and limit meat products such as hot dogs and sausage; eat organic food; eat a diet high in antioxidants (59) Occupational exposures Asbestos Laryngeal, lung, mesothelioma Prohibit use of asbestos in the home and at work; ban export of asbestos; provide asbestos awareness training; provide medical surveillance to workers exposed to asbestos (11, 21) Wood dust Lung, nasal and nasopharynx Encourage or require that workers/supervisors install exhaust ventilation system with collectors placed at points where dust is produced; provide personal protective equipment to reduce wood dust exposure; require wearing of respirators to remove hazardous particulates (dusts) (60) Petroleum products, motor vehicle exhaust (eg, diesel, PAHs, soot, and dioxins) Lung, NHL, soft-tissue sarcoma, skin Increase use of renewable products; perform thermal treatment of waste and clean coal technologies; minimize children’s exposure to toxins (11, 21) Metals (arsenic) Bladder, lung, skin, soft-tissue sarcoma of the liver Reduce exposure to arsenic in food and in safe drinking water and air (53) Reactive chemicals (vinyl chloride) Liver and biliary, soft-tissue sarcoma (angiosarcoma of the liver) Limit chronic or long-term exposure to vinyl chloride; limit use of polyvinyl chloride plastic containers and food packaging; encourage industrial workers in close contact with vinyl chloride to use respirators and wear protective clothing; avoid tobacco smoke (61, 62) Solvents (benzene) Leukemia, NHL Ensure that workers know that if benzene was released indoors, they should go out of the building; if outdoors, should leave the area and move to an area with fresh air; if exposed to benzene, should remove and dispose their clothes, rapidly wash their entire body with soap and water, and get medical care as quickly as possible; practice use of effective personal protective equipment such as breathing protection, helmet with fresh air supply, and face covering operating with positive pressure to blow clean air from inside helmet (47, 63–65) Radiation (ionizing) Bone, brain and central nervous system, breast, leukemia, liver and biliary, lung, multiple myeloma, soft-tissue sarcoma, skin, thyroid Design public policies to avoid unnecessary exposure, including legislation to promote appropriate use of radiological medical procedures; educate physicians to promote use of referral guidelines as decision-making tools to justify diagnostic procedures of choice; educate and train imaging professionals (radiologists and technicians) to apply diagnostic reference levels to radiological procedures to reduce radiation doses without affecting image quality; “Image Wisely”e—encourages imaging providers to limit medical radiation (eg, CT scan, X-rays) in adults; “Image Gently”—elimination of unnecessary testing to minimize radiation in children (63, 66, 67) Radiation (ultraviolet) Skin cancer (basal cell and squamous cell carcinomas) and malignant melanoma Reduce exposure to sun and increase provision of shade in public areas, especially for children and adolescents; encourage people to increase use of sunscreen and avoid using tanning lamps or beds (16, 35) Exposure factors . Selected risk factors associated with exposureb . Selected outcomes of exposurec . Selected potential primary intervention measures for the exposured . Reference . Environmental carcinogens Nitrates in drinking water Leukemia, bladder, lymphoma, and colorectal cancer Use treatment processes such as installation of ion exchange resin; distillation; reverse osmosis system (52) Motor vehicle exhaust (nitrogen dioxide) Childhood leukemia, central nervous system cancers Reduce outdoor air pollution from motor vehicle traffic by improving infrastructure that supports public transportation, bikeable roads, and other alternatives; use traffic controls that reduce congestion and idling; improve measures to reduce the number of vehicles on the road, such as telecommuting, flexible work hours, and rideshares, and commuting by bicycle (14, 42, 53–55) Indoor air pollutantsb Childhood leukemia and lymphoma cancers Ban of smoking cigarettes in indoor workplaces, public transportation, and indoor public places; reduce burning of wood, incense, or candles and use of gas cooking and heating appliances; reduce workers’ exposure to contaminated air at smokehouses, trash incineration facilities, oil refinery plants, and coal tar and asphalt production plants (53, 56, 57) Environmental organic pollutants (in utero) or POPs Testicular cancer Regulate carcinogenic chemicals such as exposure to pesticides; minimize exposure to POPs through ingestion and inhalation; encourage people of reproductive age to avoid eating large fish, fatty meat, and dairy products that have relatively high levels of POPs and to increase consumption of fibrous foods and green vegetables such as spinach and kale (23, 58) Pesticides such as dioxins Childhood leukemia and lymphoma, brain tumors, germ cell tumors, Hodgkin, NHL Reduce use of pesticides in residential lawns and gardens; reduce direct exposure to pesticides by children; reduce use of pesticides in agricultural products, foods, and drinking water (21, 53) PAHs Lung cancer Encourage people to reduce consumption of smoked and charbroiled foods; avoid exposure to dust, fumes, and skin contact by wearing protective clothing, such as long-sleeve shirts, long pants, and gloves when working with products containing PAHs; eliminate exposure to tobacco smoke; avoid cooking food at very high temperatures and avoid contact of foods with open flames (22) Nitrate consumption Bladder cancer Encourage people to minimize consumption of processed foods and limit meat products such as hot dogs and sausage; eat organic food; eat a diet high in antioxidants (59) Occupational exposures Asbestos Laryngeal, lung, mesothelioma Prohibit use of asbestos in the home and at work; ban export of asbestos; provide asbestos awareness training; provide medical surveillance to workers exposed to asbestos (11, 21) Wood dust Lung, nasal and nasopharynx Encourage or require that workers/supervisors install exhaust ventilation system with collectors placed at points where dust is produced; provide personal protective equipment to reduce wood dust exposure; require wearing of respirators to remove hazardous particulates (dusts) (60) Petroleum products, motor vehicle exhaust (eg, diesel, PAHs, soot, and dioxins) Lung, NHL, soft-tissue sarcoma, skin Increase use of renewable products; perform thermal treatment of waste and clean coal technologies; minimize children’s exposure to toxins (11, 21) Metals (arsenic) Bladder, lung, skin, soft-tissue sarcoma of the liver Reduce exposure to arsenic in food and in safe drinking water and air (53) Reactive chemicals (vinyl chloride) Liver and biliary, soft-tissue sarcoma (angiosarcoma of the liver) Limit chronic or long-term exposure to vinyl chloride; limit use of polyvinyl chloride plastic containers and food packaging; encourage industrial workers in close contact with vinyl chloride to use respirators and wear protective clothing; avoid tobacco smoke (61, 62) Solvents (benzene) Leukemia, NHL Ensure that workers know that if benzene was released indoors, they should go out of the building; if outdoors, should leave the area and move to an area with fresh air; if exposed to benzene, should remove and dispose their clothes, rapidly wash their entire body with soap and water, and get medical care as quickly as possible; practice use of effective personal protective equipment such as breathing protection, helmet with fresh air supply, and face covering operating with positive pressure to blow clean air from inside helmet (47, 63–65) Radiation (ionizing) Bone, brain and central nervous system, breast, leukemia, liver and biliary, lung, multiple myeloma, soft-tissue sarcoma, skin, thyroid Design public policies to avoid unnecessary exposure, including legislation to promote appropriate use of radiological medical procedures; educate physicians to promote use of referral guidelines as decision-making tools to justify diagnostic procedures of choice; educate and train imaging professionals (radiologists and technicians) to apply diagnostic reference levels to radiological procedures to reduce radiation doses without affecting image quality; “Image Wisely”e—encourages imaging providers to limit medical radiation (eg, CT scan, X-rays) in adults; “Image Gently”—elimination of unnecessary testing to minimize radiation in children (63, 66, 67) Radiation (ultraviolet) Skin cancer (basal cell and squamous cell carcinomas) and malignant melanoma Reduce exposure to sun and increase provision of shade in public areas, especially for children and adolescents; encourage people to increase use of sunscreen and avoid using tanning lamps or beds (16, 35) a Source: authors’ compilation. This table provided more details on one of the exposure factors (environmental and occupational) presented in the figure. NHL = non-Hodgkin’s lymphoma; PAH = poly-aromatic hydrocarbon; POP = persistent organic pollutant. b Selected risk factors associated with exposure (carcinogenic agent) based on a Group 1 designation by the International Agency for Research on Cancer (44, 49, 50). c Selected outcomes of the exposure are those classified as “strong evidence” of causal link to the carcinogenic agent based on a Group 1 designation by the International Agency for Research on Cancer (44, 49, 50). d The effectiveness and economic impact of some of these environmental and occupational primary prevention measures have not been quantified. This is partly due to lack of data. With data, health economics research can help quantify their economic benefits. e Image Wisely encourages imaging providers to 1) optimize use of radiation to use only the radiation necessary to produce diagnostic quality images; 2) convey the principles of the Image Wisely initiative to the imaging team to ensure that the facility optimizes its use of radiation when imaging patients; 3) communicate optimal patient imaging strategies to referring physicians and be available for consultation; and 4) routinely review imaging protocols to ensure the use of the least amount of radiation necessary to acquire a quality diagnostic image (63, 67). Open in new tab Behavioral Factors Like environmental and occupational determinants of cancer, behavioral factors also substantially contribute to the initiation and progression of cancer in humans. Examples of some of the cancers caused by behavioral factors and their recommended interventions are presented in Table 3. These behavioral factors include tobacco use, alcohol consumption, diet, nutrition, and physical activity. For decades, it has been well established that cigarette smoking causes several types of cancer (15,69,70,79), and it is associated with approximately 25% to 30% of all cancer deaths (20,28,29). Among these cancers, smoking accounts for approximately 90% of lung cancer deaths (12,28). Additionally, it has been documented that nonsmokers who are exposed to secondhand smoke have an elevated risk of being diagnosed with lung cancer (13). Like tobacco use, alcohol consumption is also a well-established modifiable risk for many cancers (71,80). Similarly, based on information from the Continuous Update Project Panel and other studies, unhealthy diet, lack of physical activity, and other sedentary behaviors contributed to increased overweight and obesity, which are associated with many types of cancer (12,74,77). It is worth noting that a few studies have reported harmful impact on health due to deliberate weight loss for people who are overweight with a body mass index of 35 kg/m2 or less (81). On the other hand, there is consistent evidence that a high body mass index is associated with increased risks of at least 13 types of cancer, and these cancers make up 40% of all cancers diagnosed in the United States each year (77). The risk of cancer associated with behavioral factors can be reduced with many available and recommended primary prevention interventions, as presented in Table 3. These primary intervention measures can be quantified through health economics research, and the outcomes can be used as inputs to inform policy decisions. Table 3. Selected behavioral risk factors and related chronic conditions by outcomes and primary intervention measuresa,b Risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for reduce outcomes of exposure . Reference . Tobacco and smoking Lung, liver, bladder, larynx, renal parenchyma, penis, oropharynx, oropharyngeal, anus, renal pelvis, stomach, uterus, pancreas, vulva, cervical Prevent people from starting to smoke; increase combustible tobacco prices; pass comprehensive smoke-free laws; conduct antitobacco mass media campaigns; promote barrier-free access to tobacco cessation counseling and treatment; eliminate exposure to secondhand smoke (15, 69, 70) Alcohol use Stomach, colorectal, oropharynx, liver, breast (postmenopause), oesophagus (squamous cell carcinoma), larynx Screen for excessive alcohol use; increase tobacco prices; regulate concentration of alcohol retailers in an area; enhance enforcement of laws prohibiting alcohol sales to minors (<21 y); provide behavioral counseling to reduce misuse (71–73) Poor diet and nutrition Lung, colorectal, pancreas, prostate, gallbladder, esophagus, gastric, breast, endometrial, larynx, mouth, pharynx Encourage people to limit calorie-dense meals; limit sugar-sweetened beverages; reduce intake of red meat; avoid processed meats; consume diet rich in whole grains, legumes, vegetables, fruits, and spices (74–76) Overweight and obesity Colorectal, multiple myeloma, kidney, esophageal (adenocarcinoma), liver, breast (postmenopause), pancreatic, ovarian, non-Hodgkin’s lymphoma, gallbladder, upper stomach, uterine, endometrial, meningioma, thyroid Support healthy eating and active living in variety of settings: communities, worksites, schools, and early care and education facilities; encourage people to eat a healthy diet and engage in sufficient physical activity; maintain healthy weight throughout life, and reduce intake of sugar sweetened drinks (77, 78) Risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for reduce outcomes of exposure . Reference . Tobacco and smoking Lung, liver, bladder, larynx, renal parenchyma, penis, oropharynx, oropharyngeal, anus, renal pelvis, stomach, uterus, pancreas, vulva, cervical Prevent people from starting to smoke; increase combustible tobacco prices; pass comprehensive smoke-free laws; conduct antitobacco mass media campaigns; promote barrier-free access to tobacco cessation counseling and treatment; eliminate exposure to secondhand smoke (15, 69, 70) Alcohol use Stomach, colorectal, oropharynx, liver, breast (postmenopause), oesophagus (squamous cell carcinoma), larynx Screen for excessive alcohol use; increase tobacco prices; regulate concentration of alcohol retailers in an area; enhance enforcement of laws prohibiting alcohol sales to minors (<21 y); provide behavioral counseling to reduce misuse (71–73) Poor diet and nutrition Lung, colorectal, pancreas, prostate, gallbladder, esophagus, gastric, breast, endometrial, larynx, mouth, pharynx Encourage people to limit calorie-dense meals; limit sugar-sweetened beverages; reduce intake of red meat; avoid processed meats; consume diet rich in whole grains, legumes, vegetables, fruits, and spices (74–76) Overweight and obesity Colorectal, multiple myeloma, kidney, esophageal (adenocarcinoma), liver, breast (postmenopause), pancreatic, ovarian, non-Hodgkin’s lymphoma, gallbladder, upper stomach, uterine, endometrial, meningioma, thyroid Support healthy eating and active living in variety of settings: communities, worksites, schools, and early care and education facilities; encourage people to eat a healthy diet and engage in sufficient physical activity; maintain healthy weight throughout life, and reduce intake of sugar sweetened drinks (77, 78) a Source: authors’ compilation. b This table provides more details on one of the exposure factors (behavioral) presented in Figure 1. The potential primary intervention measures included in the table can be quantified through health economics research. Open in new tab Table 3. Selected behavioral risk factors and related chronic conditions by outcomes and primary intervention measuresa,b Risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for reduce outcomes of exposure . Reference . Tobacco and smoking Lung, liver, bladder, larynx, renal parenchyma, penis, oropharynx, oropharyngeal, anus, renal pelvis, stomach, uterus, pancreas, vulva, cervical Prevent people from starting to smoke; increase combustible tobacco prices; pass comprehensive smoke-free laws; conduct antitobacco mass media campaigns; promote barrier-free access to tobacco cessation counseling and treatment; eliminate exposure to secondhand smoke (15, 69, 70) Alcohol use Stomach, colorectal, oropharynx, liver, breast (postmenopause), oesophagus (squamous cell carcinoma), larynx Screen for excessive alcohol use; increase tobacco prices; regulate concentration of alcohol retailers in an area; enhance enforcement of laws prohibiting alcohol sales to minors (<21 y); provide behavioral counseling to reduce misuse (71–73) Poor diet and nutrition Lung, colorectal, pancreas, prostate, gallbladder, esophagus, gastric, breast, endometrial, larynx, mouth, pharynx Encourage people to limit calorie-dense meals; limit sugar-sweetened beverages; reduce intake of red meat; avoid processed meats; consume diet rich in whole grains, legumes, vegetables, fruits, and spices (74–76) Overweight and obesity Colorectal, multiple myeloma, kidney, esophageal (adenocarcinoma), liver, breast (postmenopause), pancreatic, ovarian, non-Hodgkin’s lymphoma, gallbladder, upper stomach, uterine, endometrial, meningioma, thyroid Support healthy eating and active living in variety of settings: communities, worksites, schools, and early care and education facilities; encourage people to eat a healthy diet and engage in sufficient physical activity; maintain healthy weight throughout life, and reduce intake of sugar sweetened drinks (77, 78) Risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for reduce outcomes of exposure . Reference . Tobacco and smoking Lung, liver, bladder, larynx, renal parenchyma, penis, oropharynx, oropharyngeal, anus, renal pelvis, stomach, uterus, pancreas, vulva, cervical Prevent people from starting to smoke; increase combustible tobacco prices; pass comprehensive smoke-free laws; conduct antitobacco mass media campaigns; promote barrier-free access to tobacco cessation counseling and treatment; eliminate exposure to secondhand smoke (15, 69, 70) Alcohol use Stomach, colorectal, oropharynx, liver, breast (postmenopause), oesophagus (squamous cell carcinoma), larynx Screen for excessive alcohol use; increase tobacco prices; regulate concentration of alcohol retailers in an area; enhance enforcement of laws prohibiting alcohol sales to minors (<21 y); provide behavioral counseling to reduce misuse (71–73) Poor diet and nutrition Lung, colorectal, pancreas, prostate, gallbladder, esophagus, gastric, breast, endometrial, larynx, mouth, pharynx Encourage people to limit calorie-dense meals; limit sugar-sweetened beverages; reduce intake of red meat; avoid processed meats; consume diet rich in whole grains, legumes, vegetables, fruits, and spices (74–76) Overweight and obesity Colorectal, multiple myeloma, kidney, esophageal (adenocarcinoma), liver, breast (postmenopause), pancreatic, ovarian, non-Hodgkin’s lymphoma, gallbladder, upper stomach, uterine, endometrial, meningioma, thyroid Support healthy eating and active living in variety of settings: communities, worksites, schools, and early care and education facilities; encourage people to eat a healthy diet and engage in sufficient physical activity; maintain healthy weight throughout life, and reduce intake of sugar sweetened drinks (77, 78) a Source: authors’ compilation. b This table provides more details on one of the exposure factors (behavioral) presented in Figure 1. The potential primary intervention measures included in the table can be quantified through health economics research. Open in new tab Description of Existing Primary Prevention Interventions for Each Exposure Factor to Reduce the Incidence of Cancer Because of the complex process in which cancer develops in humans, it may be impossible to know the full range of agents or combination of agents that can cause cancer. However, it is well documented that the majority of exposures associated with initiation and development of cancers in humans are preventable (13,15,68). A study by DeVita et al. (15) chronicled important events in the past 200 years in cancer prevention. These events include progress in chemoprevention and in discoveries of interactions between infectious agents and cancer as well as discoveries of the impact of tobacco use in cancer disease. Based on these discoveries, advances in environmental and occupational health research, and a better understanding of the factors that influence behavioral choices in the past decades, there are many evidence-based recommendations to eliminate or reduce the presence, use, or consumption of cancer-causing carcinogenic agents (16,33,35,36,39,42,44,48,58,70–72,78,82). These recommendations have been promulgated by entities such as the US Preventive Services Task Force, the Advisory Committee on Immunizations Practices, the Food and Drug Administration, the Environmental Protection Agency, the Community Preventive Services Task Force (CPSTF), and the World Cancer Research Fund/American Institute for Cancer Research (16,33,35,36,39,42,44,48,58,70–72,74,78,82). The preventive interventions recommended by these organizations have proven to be an essential aspect of disease prevention and health promotion in the US, but they are consistently underused (83,84). According to the US Preventive Services Task Force, genetic counseling and testing are recommended for individuals at increased risk of certain cancers associated with inherited genetic mutations (33–35). The recommendations requires that counseling include a full explanation of the risks and benefits of genetic testing, informed consent, and psychosocial issues that may extend beyond those encountered in a general oncology office (33–35). An increase in the proportion of females at higher risk of breast or ovarian cancer who receive genetic counseling is one of the Healthy People 2030 developmental objectives on cancer preventive care (85). For cancers caused by infectious agents, the recommended set of primary prevention interventions includes prophylactic vaccines for preventing HPV and hepatitis B virus (38,40–42) and treatment for H. pylori, hepatitis C virus, HIV, and other cancer-causing infections (39,43,44). Many primary prevention interventions shown to be effective in eliminating or decreasing exposure to environmental and occupational carcinogens have been identified. Many of these interventions are listed in the World Health Organization’s “Primary prevention of cancer through mitigation of environmental and occupational determinants” (86). Similarly, a systematic study by Espina et al. (87) presented an evidence-based global strategy for the primary prevention of environmental and occupational cancers. The economic impact of some of these environmental and occupational prevention measures in reducing the initiation and progression of cancer has not been quantified (Table 2). Primary interventions to eliminate or reduce the harmful impact of behavioral factors, including tobacco use, alcohol consumption, unhealthy diet, and physical inactivity, that are associated with the initiation of cancer have been discussed by multiple organizations and investigators (Table 3) (71,72,88). Some of these preventive interventions involve direct economic activities, such as increasing the price of alcohol, sugar-sweetened beverages, or combustible tobacco, often through excise taxes (70–72). Other interventions have indirect economic effects, such as creating barriers to access to alcohol, combustible tobacco, or foods low in nutritional value, or, conversely, increasing access to affordable, healthy foods and environments for physical activity (70–72,74,75,78). Although the effectiveness of many primary prevention interventions has been documented, more information about their economic evidence to inform both the short- and long-term resource allocation decisions to reduce cancer incidence is needed. Gaps and Unmet Needs in Health Economics Research Focused on Primary Prevention of Cancer Although primary prevention can be an effective and cost-effective approach for reducing the risk of cancers caused by exposures described earlier, multiple knowledge gaps regarding factors affecting the economics of primary prevention of cancer remain. For example, primary prevention interventions may occur years (or decades) before a targeted population is at the highest risk of developing cancer associated with the prevented activities or risk factors. Collecting robust data linking primary prevention interventions and subsequent cancer incidence is therefore extremely challenging and may be expensive. More research could help link short- and intermediate-term changes in risk factors and health outcomes from prevention interventions to longer-term outcomes and increase the use of modeling to better project primary intervention effects. In addition to documenting outcomes from prevention interventions, the costs of conducting primary prevention interventions are also often not well documented. When such costs are assessed, they may be based on rough estimates from salaries of intervention personnel and supplies used rather than on more detailed assessments of the value of all the resources required to deliver the intervention. Cancer health economics researchers may want to partner with implementation scientists to better assess the processes and associated costs for implementing and disseminating interventions that have been shown to be effective in pilot studies. For example, in the CPSTF recommendations, health economists regularly work with epidemiologists and medical officers to quantify the cost-effectiveness of prevention interventions that have been found to be effective (89,90). This type of collaborative work could support primary prevention of cancer interventions. One critical gap is that many policy interventions to prevent cancer are understudied in the United States because it is not possible to link policy exposure to survey or administrative data that could help to evaluate both intended and unintended effects of the intervention. For instance, the link between how disparities in cancer risk factors translate into economic and health disparities in the population is understudied. Geocodes may be needed for these linkages but may not be available because of concerns over patient confidentiality. One potential option would be to provide publicly available data aggregated by geography (eg, state), which would be enough to permit many policy intervention studies without compromising data security. In addition, some of the critical information needed to analyze the economics of primary prevention of cancer interventions may not be available. This may include details regarding the delivery of the primary prevention interventions, the motivations participants have for engaging in these interventions, the costs participants incur (eg, transportation, parking, childcare), and the impact of interventions on health-related beliefs and behaviors. Such gaps in information are even more problematic when attempting to evaluate the economics of prevention-focused cancer interventions among underserved populations. Medically underserved individuals may be underrepresented in available data resources, and their care may be even more fragmented. Further, social determinants of health (SDoH) may have particularly important effects on the economics of cancer prevention for individuals from racial and ethnic minority groups, people with lower incomes, people who live in rural areas, and other populations at increased risk for cancer, but information on SDoH may be incomplete or missing from available data. Better collection of standardized SDoH data and data on social needs and social risk factors could help address these gaps in the future. With enhanced collection of standardized SDoH data, health economics researchers can develop models to better project associations between socioeconomics determinants (inequalities and inequities) and potential interventions for the primary prevention of cancer. These models can then be used to tailor interventions to improve the effectiveness and cost-effectiveness of interventions for the primary prevention of cancer among populations that are medically underserved or at higher risk of cancer. In addition, programs can be developed to improve daily living conditions, tackle unequal distribution of resources, and estimate the cost vs benefit of interventions for the primary prevention of cancer (eg, education vs taxation targeting excess alcohol consumption) in different communities. An additional unmet need in prevention-focused cancer health economics research is timely involvement of community-based organizations. Many existing prevention interventions require community engagement for participant recruitment, intervention delivery, and accurate follow-up. However, some researchers may not engage community leaders or community-based organizations early in the development of intervention plans, potentially compromising cost-effectiveness as well as potential relevance or usefulness to the intended recipients, while also potentially restricting the population that can receive the intervention. Similarly, the development of important collaborations between cancer health economics researchers and community-based advocates or policy makers interested in cancer prevention may be of benefit. Researchers may need to learn to communicate with nonresearcher audiences to help address these unmet needs. Training is also an important unmet need for health economics research focused on cancer prevention. Efforts could be made to improve training among both undergraduate and graduate students as well as among clinical trainees. This includes interdisciplinary or cross-disciplinary training, bringing together economists, health services researchers, decision scientists, epidemiologists, statisticians, clinicians, and others. Training could be enhanced through collaborations between economics departments, schools and programs of public health, medical schools, public health agencies, and other allied health departments. Because primary prevention intervention research involves a community focus, it is therefore critical that this training also involve a community focus. Such training can include partnerships with community-based organizations and advocates, policy makers, and government officials, and provide experience in community-based participatory research. In addition to helping advance the field of cancer health economics research and address the challenges of studying primary prevention, improving training opportunities could help research professionals learn new methods and develop new approaches. The 1971 National Cancer Act contributed to the growth and evolution of health economics research in NCI. A few studies in this special supplement provided information on the history and funding of health economics research in NCI (90,91). However, many important aspects in economics of primary prevention of cancer have not been addressed through NCI funding. Funding opportunity announcements or notice of special interests could be further developed to foster more research in health economics. Because health economics methods vary considerably across subspecialties, study section reviewers need to be carefully chosen. For example, a health economist with expertise in natural experiments may not be an appropriate reviewer for a cost-effectiveness study and vice versa. Collaborations between individuals from diverse disciplines should be encouraged because cancer health economics research is a transdisciplinary field. These collaborations can draw on knowledge from “team science” by bringing together researchers who may not share common methods, scientific approaches, or even research vocabularies (92). In addition, efforts to enhance dissemination of health economics research findings on primary prevention would be valuable to nonresearcher audiences such as policy makers and community leaders, who are often key for gaining widespread interest and engagement in cancer prevention activities. Additionally, knowledge translation of economic research for communication to advocates, health practitioners, decision makers, and the target population is also underserved. Challenges in Conducting Health Economics Research Focused on Primary Prevention of Cancer The outcome of prevention is not immediate (17). This is a challenge most health economists conducting health economics research on primary prevention of cancer know too well. Cancer as a disease develops slowly, so it takes years or decades to observe the impact of primary intervention efforts. As such, the benefits of the intervention may become difficult to be accounted for and to be credited to the payer of the prevention. Further, primary prevention guidelines are constantly changing and in some cases are inconsistent. For example, some guidelines provide limits for moderate alcohol consumption, whereas others report that any amount of alcohol use is harmful to human health (93). Activities to reduce the development of cancer can continue throughout the lifespan (10,18). Also, some aspects of primary prevention may be expensive; even when primary prevention is inexpensive (or free), individuals may have personal conflicts such as religious or cultural beliefs that restrict them from participating in an intervention. Based on these and other impediments, it is often challenging to estimate the true economic costs and benefits of primary prevention of cancer. Other challenges faced by health economics researchers is the reliance on quasi- or natural experimental study designs to establish a causal link between health outcome and primary prevention interventions. However, natural experiments involving cancer are often infrequent and potentially of limited generalizability. Hence, researchers use observational studies based on existing databases that may have dated information and are inadequate to convert health outcomes into policy recommendations that can be implemented to improve population health. A related challenge is data accessibility. Individuals may receive cancer-focused preventive care (eg, HPV or hepatitis B vaccination, smoking prevention, or cessation interventions, etc) through 1 health-care system or while covered by 1 type of health insurance. They will likely see health-care providers affiliated with multiple other health-care systems and be covered by other types of health insurance throughout their lives. Being able to access these fragmented pieces of health information about individuals could be a substantial barrier to conducting cancer health economics research focused on primary prevention. Even when more comprehensive data are available, for example, from an all-payer claims data resource, the cost of accessing such data may be prohibitive. As previously described, geographic data are also needed to conduct natural experiment–style studies of policy changes. Because of the issues highlighted above, in general, primary prevention of cancer may not be fully accepted in the private sector for commercial interests. The business case for primary prevention of cancer interventions is different from that related to cancer screening, treatment, and survivorship care. Opportunities in Health Economics Research Focused on Primary Prevention of Cancer Amid the challenges in conducting health economics research on primary prevention of cancer, there are also many opportunities, which may be classified into 2 broad approaches: economic evaluation and applied micro-econometric research. Within these 2 broad areas, there are many methods and approaches economists have used over the years to estimate the costs and benefits of primary prevention of cancer. Some of these methods and approaches are discussed below. Economic Evaluation Economic evaluations require consideration of the costs and consequences of various interventions for cancer prevention. The method includes cost-effectiveness analysis, cost-utility analysis, and cost-benefit analysis, and all are well recognized and have been used to quantify the benefits of primary prevention of cancer interventions (90,94). Using these methods, health economists have an opportunity to provide inputs that decision makers can consider to effectively allocate health prevention resources based on many factors that may include individual or group preference. For example, outcomes from health economic evaluations can reveal that some population groups are more likely to have occupations that put them at increased risk of exposure to carcinogenic agents. This outcome may be one of the inputs that decision makers would consider in allocating prevention resources to different segments of the population. Further, as an area of growing interest, economists have an opportunity to work with clinicians in adding an economic component to randomized clinical trials that can provide timely data on both costs and health outcomes. The data can be used as part of the input to evaluate the costs and benefits of the trials to the population being studied. Similarly, as the CPSTF has begun to incorporate economic evaluation information into the development of their respective evidence-based recommendations for health services (89,90), health economists have an opportunity to help interpret the economic data in these guidelines to decision makers at all levels. The ability to use the available cancer registry data (95) is an important opportunity for economic evaluations of cancer prevention. The registry data, combined with sophisticated decision analysis models, can allow for rigorous estimates of the effect of primary cancer interventions on short- and long-term outcomes (Figure 1). Applied Micro-Econometric Research In past decades, advances in data science and economic methods have offered exciting new opportunities in applied micro-econometric health economics research in primary prevention of cancer (96,97). This approach provides evidence about the causal relationships between specific cancer risk factors and outcomes. It can also allow causal inferences about the links between primary prevention of cancer, public policies, and SDoH. For example, micro-econometric research could estimate whether policies that regulate alcohol retail stores in an area (eg, neighborhood or city) could reduce alcohol consumption and prevent certain cancers. These advances in data and methods are fueling more opportunities for health economists to use state-of-the-art applied micro-econometric methods and credible research designs, including difference-in-difference, instrumental variables, regression discontinuity, and synthetic control methods, to evaluate the benefits of primary prevention of cancer interventions (98). Further, advances in data and methods have provided more opportunities for cancer health economists to 1) quantify the causal impacts of primary prevention of cancer to reduce common health conditions such as obesity, diabetes, and certain infectious diseases; 2) estimate the causal impacts of addressing socioeconomic, biological, and other factors that contribute to higher cancer rates in specific population groups; 3) leverage unconventional sources of data to identify and estimate the causal impacts of new primary cancer interventions deemed to reduce cancer risk; and 4) estimate the interactions of costs and cost-effectiveness of the impact of different environmental and occupational exposures on cancer risk based on where individuals were born, live, learn, work, and play (what is known as SDoH). The unconventional sources of data for health economics study may include cellular-based measures of consumer mobility. Additional opportunities involve public–private data partnerships, such as linking SEER and MarketScan data to study etiology and risk factors of cancer in individuals younger than 65 years who are members of specific populations. Further, in recent years, data scientists have developed variable selection methods, including least absolute shrinkage and selection operator (LASSO), regression trees, and random forests (97), which offer more opportunities for health economists to apply these new methods in studying primary prevention of cancer. Another opportunity for health economics research in primary prevention of cancer could be to use machine-learning (96) and big data methods (97) to estimate the causal impacts of novel preventive interventions. For example, recent studies have reported evidence that a substantial proportion of cancers are developed through chronic inflammation, which is linked to various steps involved in tumorigenesis (99–103). There may be multiple types of primary prevention opportunities to address chronic inflammation that can be identified using these advanced approaches as well as a corresponding need to assess their associated causal impacts. Another opportunity for health economics research is the need to incorporate the impacts of macroeconomic factors in primary prevention of cancer. Many of the modifiable risk factors discussed in this article (poor diet, physical inactivity, tobacco use, harmful alcohol consumption, and occupational and environmental exposures) have negative impacts on employment, national productivity, and health insurance coverage. A recent systematic review reported evidence of little attention devoted to macroeconomic impacts associated with noncommunicable disease, including cancer prevention (104). With advances in data science, health economists can use prevention impact models to estimate causal linkages of cancer risk factors, macroeconomic burden, and primary prevention of cancer. Future Directions for Enhancing Health Economics Research on Primary Prevention of Cancer The continued declines in annual cancer death rates in the past 2 decades are a strong indication of progress in cancer control (1), including the role of primary prevention. For example, many reports have credited tobacco prevention and control efforts as one of the major contributing factors to substantial decline in lung cancer (15,79,105). On the other hand, in recent years, we have observed rising incidence rates of some cancers associated with behavioral factors such as alcohol consumption, high sugar consumption leading to excess body weight, and physical inactivity (74,75,77). The rising incidence of these cancers makes a compelling case for improvements in prevention and in health economics research to quantify the outcomes of primary prevention of cancer interventions. Health economic outcomes may serve as an aid to raise awareness, guide recommendations for preventive action, prioritize resources, assist in policy development, and prepare models to monitor the long-term impacts of primary prevention of cancer. Economic decision models in particular serve these roles by acting as comprehensive evidence reviews that bring together disparate data sources to quantify the health and financial benefits and potential side effects of primary prevention. Based on the existing gaps, needs, challenges, and opportunities in health economics research in primary prevention of cancer, the following considerations are offered as potential next steps. First, because of the complex interactions of preventable factors causally associated with the development of cancer, health economics research has an integral role to play to quantify the costs and benefits of primary prevention of cancer interventions, programs, and policies. Building the economic evidence base contemporaneously with the evidence base on cancer risk factors and intervention effectiveness may speed appropriate adoption of primary prevention of cancer interventions. This effort would benefit from improvements in data modernization, training of the workforce, and methods related to health economics in basic and applied research. Second, it has been reported that the impacts of primary prevention of cancer interventions for most environmental and occupational exposures found to be convincing or probable evidence of carcinogens to humans have not been quantified (20,86). This gap could be addressed with multidisciplinary collaborative teams involving health economists, epidemiologists, toxicologists, and individuals from other disciplines to collect appropriate data and develop appropriate methods to quantify the health and economic benefits of interventions that can eliminate or decrease exposures to specific environmental and occupational carcinogens. Third, because of the COVID-19 pandemic, access to many preventive interventions such as tobacco cessation programs, healthy foods, and physical activity has been substantially reduced, and this may affect longer-term health outcomes (106). Health economists can use different economic methods to guide decisions on the health benefits of continued primary prevention of cancer interventions during or after a pandemic like COVID-19 or any other natural disaster. Finally, health economics researchers can apply existing methods or develop new ones to examine how health literacy may affect the efforts of primary prevention of cancer. This could be invaluable in generating new knowledge that can promote the optimal design of primary prevention of cancer interventions to populations that are medically underserved or populations that have been economically or socially marginalized. These and other forms of social inequities contribute to health disparities, which have been amplified during the COVID-19 pandemic (107,108). Related to this, cancer health economics researchers could use findings from their research to communicate broadly and in appropriate formats to community-based partners and relevant policy makers. Conclusions Health economics is a discipline with a unique role in quantitative evaluation of public health interventions. Specifically, the field has an important role in adding to the evidence used to evaluate the business case for primary prevention of cancer. This requires providing valid and credible information on the costs and benefits of a wide range of preventive measures, such as reducing tobacco use and consumption of foods low in nutritional value, controlling infectious virus and bacteria through vaccination and treatment, avoiding intensive sun exposure, decreasing sedentary behavior, reducing alcohol consumption, and reducing environmental and occupational exposures to carcinogenic agents. Maximizing the potential contribution of the field of health economics to primary cancer prevention can be supported by modernization of data systems, enhanced training of the health economics workforce, improvements in analytic methods, and increased opportunities for interdisciplinary collaboration. With time, these efforts can help to promote overall health in the short term and reduce cancer incidence and morbidity in the long term. Funding No funding was received for this commentary. Notes Role of the funder: Not applicable. Disclosures: The authors indicate no conflicts of interest. Author contributions: Conceptualization: DUE, MTH, DSK. Project administration: DUE. Visualization: DUE, MTH, DSK. Writing, original draft: DUE, MTH, DSK. Writing, review, and editing: DUE, MTH, DSK, HWC, MA, JD, YRH, MM, MFP. Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. Prior presentation: Some of this content was presented at the 2020 Future of Cancer Health Economics Research virtual conference. References 1 Islami F , Ward EM, Sung H, et al. Annual report to the nation on the status of cancer, part 1: national cancer statistics . 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Health Economics Research in Primary Prevention of Cancer: Assessment, Current Challenges, and Future Directions

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Oxford University Press
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Copyright © 2022 Oxford University Press
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1052-6773
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1745-6614
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10.1093/jncimonographs/lgac014
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Abstract

Abstract In the past 2 decades, the demand for information on health economics research to guide health care decision making has substantially increased. Studies have provided evidence that eliminating or reducing tobacco use; eating a healthy diet, including fruit and vegetables; being physically active; reducing alcohol consumption; avoiding ultraviolet radiation; and minimizing exposure to environmental and occupational carcinogenic agents should substantially reduce cancer incidence in the population. The benefits of these primary prevention measures in reducing cancer incidence are not instantaneous. Therefore, health economics research has an important role to play in providing credible information to decision makers on the health and economic benefits of primary prevention. This article provides an overview of health economics research related to primary prevention of cancer. We addressed the following questions: 1) What are the gaps and unmet needs for performing health economics research focused on primary prevention of cancer? 2) What are the challenges and opportunities to conducting health economics research to evaluate primary prevention of cancer? and 3) What are the future directions for enhancing health economics research on primary prevention of cancer? Modeling primary prevention of cancer is often difficult given data limitations, long delays before the policy or intervention is effective, possible unintended effects of the policy or intervention, and the necessity of outside expertise to understand key inputs or outputs to the modeling. Despite these challenges, health economics research has an important role to play in providing credible information to decision makers on the health and economic benefits of primary prevention of cancer. In the past decades, the overall annual cancer death rates have continued to decline for all cancer sites combined (1), and the United States is making substantial progress in reducing cancer death rates, as evident in the meeting of Healthy People 2020 targets (2). However, changes in cancer incidence rates were mixed, with new cases leveling off in men and slightly increasing in women (1). Similarly, during the past 5 years, the overall cancer incidence rates in children 15 years and younger, adolescents, and young adults have increased (1). Cancer remains the second leading cause of death in the United States (3), with substantial negative outcomes to quality of life and life expectancy. In addition to the health burden, cancer also has substantial economic impacts on patients, their families, caregivers, employers, and the health-care system. For example, in a recent study, medical care costs for cancer in the United States were estimated to be $185 billion in 2015 and were projected to increase to more than $240 billion by 2030 based only on population growth (4). As a result, efforts to prevent new cases of cancer are paramount to substantially reducing cancer-related mortality. These efforts would likely benefit from concerted resources devoted to primary prevention, keeping people healthy and cancer free. In general, preventing health conditions such as cancer involves at least 3 broad categories: primary, secondary, and tertiary prevention (5). Primary prevention focuses on interventions to lower cancer risk so fewer cases of cancer ever occur. An example of such an intervention is the human papillomavirus (HPV) vaccination to prevent infection and the subsequent occurrence of HPV-associated cancers (cervical, oropharyngeal, vulva, vagina, penis, anus). Secondary prevention seeks to prevent the progression of cancer by focusing on interventions such as screening and early detection of cancer. An example of such an intervention is mammography for breast cancer screening. The final category is tertiary prevention, which aims to reduce death or severity of cancer in an individual through clinical interventions such as treatment and rehabilitation. This study focuses on primary prevention. This article is part of a collection of articles on “The Future of Cancer Health Economics Research,” a virtual conference sponsored and hosted by the National Cancer Institute (NCI) in December 2020. In this article, the Primary Prevention of Cancer Planning Group (Planning Group) was charged to focus on 1 aspect of the cancer control continuum: prevention (6). Other planning groups within the virtual conference focused on different areas of the cancer control continuum (ie, screening, treatment, and survivorship). Articles on these areas of the cancer control continuum are included in the collection (7-9). All planning groups were charged to address the following issues: 1) What are the gaps and unmet needs for performing health economics research focused on cancer? 2) What are the challenges and opportunities to conducting cancer health economics research? and 3) What are the future directions for enhancing health economics research to address these needs and support primary cancer prevention? In this article, we take a broad approach to our description of cancer health economics research. This includes 1) economic evaluations that provide evidence that guides how to allocate scarce resources most efficiently for cancer prevention, and 2) applied micro-econometric research that provides evidence about the causal relationships between specific cancer risk factors and outcomes. Methods Before the December 2020 virtual conference, the Primary Prevention of Cancer Planning Group convened several meetings from August to November 2020. The planning group consisted of health economists and health services researchers who are experts in cancer control, sexually transmitted infections, tobacco use, and other health conditions or behaviors related to primary prevention of cancer. Group members came from different organizational and institutional settings. To guide our deliberation and discussions, the planning group proposed a framework for the economics of primary prevention of cancer (Figure 1) to supplement the previously published framework on cancer health economics research (6). Figure 1. Open in new tabDownload slide Framework for conducting health economics research on primary prevention of cancer. *Stages of lifespan were adopted from the CDC’s Preventing Cancer Across a Lifetime initiative (10). Figure 1. Open in new tabDownload slide Framework for conducting health economics research on primary prevention of cancer. *Stages of lifespan were adopted from the CDC’s Preventing Cancer Across a Lifetime initiative (10). In the proposed framework, the planning group recognized that cancer is caused by a complex web of multiple factors that are multi-stage in nature (11). As such, it may be impossible to identify all the factors that could be addressed by primary prevention. However, the planning group identified 3 broad factors that encompass all aspects of cancer related to prevention: 1) genetic and biological, 2) environmental and occupational, and 3) behavioral. For each of these factors, several epidemiological and behavioral studies have reported evidence of interventions to reduce the incidence of cancer (12-16). Despite strong evidence for the effectiveness of prevention, gaps remain in health economics research on primary intervention to reduce cancer incidence. According to Harvey Fineberg, the former President of the National Academy of Medicine (formerly the Institute of Medicine), the gap exists because “Prevention is a hard sell” (17). He stated, “There is no drama in prevention; non‐events are not counted; statistical lives don’t have immediacy; […]; prevention often runs against commercial interests; it may conflict with personal preferences or religious beliefs; and there is declining trust in leaders and institutions challenging people’s willingness to follow guidelines” (17). These issues articulated by Feinberg are part of the case for the economics of primary prevention. For instance, in the past 30 years, only 7.1% of health economic studies in which the outcomes were measured in quality-adjusted life-years gained in cancer disease were conducted in primary prevention compared with 68.4% of studies conducted in tertiary prevention. In this article, first, we describe primary prevention of cancer. Second, we identify existing primary prevention interventions to prevent or reduce the incidence of cancer. Third, we describe the gaps and unmet needs for performing health economics research focused on primary prevention of cancer. Fourth, we address the challenges to conducting cancer health economics research. Fifth, we discuss the opportunities to conduct health economics research focused on primary prevention of cancer. Finally, we discuss future directions for enhancing and supporting primary prevention of cancer health economics research. Factors That Can Increase Cancer Risk Many factors can contribute to the risk of developing cancer over a lifetime. These may include foods and beverages we consume, chemicals and radiation we are exposed to, and viruses and bacteria we encounter (18). Cancer risk can be influenced by endogenous factors such as inherited genes, hormones, immunologic conditions, and other characteristics of individuals such as age and sex (19). Exogenous (environmental) factors affecting cancer risk may occur in occupational or home settings and involve socioeconomic status, behavioral factors, stress, and infectious agents (20). These factors interact with each other (Figure 1) and may include carcinogenic substances or effects that can damage one’s DNA, causing the initiation and progression of some cancers (21-23). The initiation and progression process can even start as early as prenatal and progress through all life stages to older adulthood (Figure 1) (24,25). For example, repeated occupational exposures to carcinogenic agents by an individual at childbearing age may increase the risk of cancer in their offspring (26). Some epidemiologists have estimated that from 30% to 50% of cancers are preventable (27–29), based on epidemiologic studies demonstrating a causal relationship with many exogenous factors (20). In addition, although age has been recognized as a nonmodifiable risk factor for cancer (30), a commentary cast doubt on the notion that cancer cannot be prevented among older adults (31). That is, age as a risk factor reflects the biology of aging as well as the cumulative effect of environmental and occupational exposures, chronic conditions (diabetes, obesity), and behavioral factors acquired during a lifetime, and these risk factors can potentially be prevented or modified. Although some cancers are associated with inherited genetic mutations (eg, certain breast and ovarian cancers, colorectal, and skin cancers), primary prevention interventions such as genetic counseling and testing can help reduce the incidence of these cancers (32,33). Some of the genes, their associated cancers, and recommended interventions are presented in Table 1. Table 1. Selected genes and infectious agents by risk factors associated with exposure, outcomes of the exposure, and primary intervention measuresa,b Exposure factors . Selected risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for the exposure . Reference . Selected genes associated with risk of each cancer Lynch syndrome (MLH1, MSH2, MSH6, PMS2, EPCAM) Colorectal cancer Chemoprevention (eg, aspirin and some vitamins), genetic counseling and genetic testing (32, 34) BRCA1 and BRCA2 Breast and ovarian cancer Genetic counseling and genetic testing, prophylactic mastectomy, chemoprevention (tamoxifen or raloxifene) (33) CDKN2A and CDK4 Malignant melanoma Protection from ultraviolet radiation, avoidance of recreational outdoor sunbathing, avoidance of tanning beds or tanning salons, prohibiting tanning bed access for minors (35) SCLC1 Lung cancer Abstinence from smoking, smoking cessation; avoidance of secondhand smoke (36) HPC1+, TLR variants Prostate cancer Chemoprevention with finasteride, dutasteride; choosing a low-fat diet (37) DPC4 Pancreatic cancerc Suggested prevention: adherence to preventive behavioral factors discussed in this article (11) Selected infectious agents HBV HCC/liver cancer Vaccination with prophylactic HBV vaccine (38) HCV HCC/liver cancer Testing and treatment with antiviral drugs (39) HPV-6, 11, 16, and 18 Cervical, vulvar, vaginal, and anal cancers and dysplasia; genital warts Vaccination with prophylactic quadrivalent HPV vaccine (40) HPV 16, 18, 31, 33, 45, 52, and 58 Cervical, oropharyngeal vulvar, vaginal, and anal cancers and dysplasia Vaccination with prophylactic 9-valent HPV vaccine (41, 42) Helicobacter pylori Gastric cancers Testing and treating with a combination of stomach acid suppressants and antibiotics (43) HIV Lymphoma; Kaposi sarcoma Testing and treating with a combination of antiviral drugs (44) Exposure factors . Selected risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for the exposure . Reference . Selected genes associated with risk of each cancer Lynch syndrome (MLH1, MSH2, MSH6, PMS2, EPCAM) Colorectal cancer Chemoprevention (eg, aspirin and some vitamins), genetic counseling and genetic testing (32, 34) BRCA1 and BRCA2 Breast and ovarian cancer Genetic counseling and genetic testing, prophylactic mastectomy, chemoprevention (tamoxifen or raloxifene) (33) CDKN2A and CDK4 Malignant melanoma Protection from ultraviolet radiation, avoidance of recreational outdoor sunbathing, avoidance of tanning beds or tanning salons, prohibiting tanning bed access for minors (35) SCLC1 Lung cancer Abstinence from smoking, smoking cessation; avoidance of secondhand smoke (36) HPC1+, TLR variants Prostate cancer Chemoprevention with finasteride, dutasteride; choosing a low-fat diet (37) DPC4 Pancreatic cancerc Suggested prevention: adherence to preventive behavioral factors discussed in this article (11) Selected infectious agents HBV HCC/liver cancer Vaccination with prophylactic HBV vaccine (38) HCV HCC/liver cancer Testing and treatment with antiviral drugs (39) HPV-6, 11, 16, and 18 Cervical, vulvar, vaginal, and anal cancers and dysplasia; genital warts Vaccination with prophylactic quadrivalent HPV vaccine (40) HPV 16, 18, 31, 33, 45, 52, and 58 Cervical, oropharyngeal vulvar, vaginal, and anal cancers and dysplasia Vaccination with prophylactic 9-valent HPV vaccine (41, 42) Helicobacter pylori Gastric cancers Testing and treating with a combination of stomach acid suppressants and antibiotics (43) HIV Lymphoma; Kaposi sarcoma Testing and treating with a combination of antiviral drugs (44) a Source: authors’ compilation. HBV = hepatitis B virus; HCC = hepatocellular carcinoma; HCV = hepatitis C virus; HPC1 = hereditary prostate cancer 1; HPV = human papilloma virus; TLR = toll-like receptor. b This table provides additional details on 1 of the exposure factors (genetics or biological) presented in Figure 1. In addition, the potential primary intervention measures included in the table can be quantified through health economics research. c Available evidence suggests that lifestyle and behavioral modifications and limiting exposure to certain chemicals in the workplace can reduce the risk of pancreatic cancer. Open in new tab Table 1. Selected genes and infectious agents by risk factors associated with exposure, outcomes of the exposure, and primary intervention measuresa,b Exposure factors . Selected risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for the exposure . Reference . Selected genes associated with risk of each cancer Lynch syndrome (MLH1, MSH2, MSH6, PMS2, EPCAM) Colorectal cancer Chemoprevention (eg, aspirin and some vitamins), genetic counseling and genetic testing (32, 34) BRCA1 and BRCA2 Breast and ovarian cancer Genetic counseling and genetic testing, prophylactic mastectomy, chemoprevention (tamoxifen or raloxifene) (33) CDKN2A and CDK4 Malignant melanoma Protection from ultraviolet radiation, avoidance of recreational outdoor sunbathing, avoidance of tanning beds or tanning salons, prohibiting tanning bed access for minors (35) SCLC1 Lung cancer Abstinence from smoking, smoking cessation; avoidance of secondhand smoke (36) HPC1+, TLR variants Prostate cancer Chemoprevention with finasteride, dutasteride; choosing a low-fat diet (37) DPC4 Pancreatic cancerc Suggested prevention: adherence to preventive behavioral factors discussed in this article (11) Selected infectious agents HBV HCC/liver cancer Vaccination with prophylactic HBV vaccine (38) HCV HCC/liver cancer Testing and treatment with antiviral drugs (39) HPV-6, 11, 16, and 18 Cervical, vulvar, vaginal, and anal cancers and dysplasia; genital warts Vaccination with prophylactic quadrivalent HPV vaccine (40) HPV 16, 18, 31, 33, 45, 52, and 58 Cervical, oropharyngeal vulvar, vaginal, and anal cancers and dysplasia Vaccination with prophylactic 9-valent HPV vaccine (41, 42) Helicobacter pylori Gastric cancers Testing and treating with a combination of stomach acid suppressants and antibiotics (43) HIV Lymphoma; Kaposi sarcoma Testing and treating with a combination of antiviral drugs (44) Exposure factors . Selected risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for the exposure . Reference . Selected genes associated with risk of each cancer Lynch syndrome (MLH1, MSH2, MSH6, PMS2, EPCAM) Colorectal cancer Chemoprevention (eg, aspirin and some vitamins), genetic counseling and genetic testing (32, 34) BRCA1 and BRCA2 Breast and ovarian cancer Genetic counseling and genetic testing, prophylactic mastectomy, chemoprevention (tamoxifen or raloxifene) (33) CDKN2A and CDK4 Malignant melanoma Protection from ultraviolet radiation, avoidance of recreational outdoor sunbathing, avoidance of tanning beds or tanning salons, prohibiting tanning bed access for minors (35) SCLC1 Lung cancer Abstinence from smoking, smoking cessation; avoidance of secondhand smoke (36) HPC1+, TLR variants Prostate cancer Chemoprevention with finasteride, dutasteride; choosing a low-fat diet (37) DPC4 Pancreatic cancerc Suggested prevention: adherence to preventive behavioral factors discussed in this article (11) Selected infectious agents HBV HCC/liver cancer Vaccination with prophylactic HBV vaccine (38) HCV HCC/liver cancer Testing and treatment with antiviral drugs (39) HPV-6, 11, 16, and 18 Cervical, vulvar, vaginal, and anal cancers and dysplasia; genital warts Vaccination with prophylactic quadrivalent HPV vaccine (40) HPV 16, 18, 31, 33, 45, 52, and 58 Cervical, oropharyngeal vulvar, vaginal, and anal cancers and dysplasia Vaccination with prophylactic 9-valent HPV vaccine (41, 42) Helicobacter pylori Gastric cancers Testing and treating with a combination of stomach acid suppressants and antibiotics (43) HIV Lymphoma; Kaposi sarcoma Testing and treating with a combination of antiviral drugs (44) a Source: authors’ compilation. HBV = hepatitis B virus; HCC = hepatocellular carcinoma; HCV = hepatitis C virus; HPC1 = hereditary prostate cancer 1; HPV = human papilloma virus; TLR = toll-like receptor. b This table provides additional details on 1 of the exposure factors (genetics or biological) presented in Figure 1. In addition, the potential primary intervention measures included in the table can be quantified through health economics research. c Available evidence suggests that lifestyle and behavioral modifications and limiting exposure to certain chemicals in the workplace can reduce the risk of pancreatic cancer. Open in new tab Certain viruses, bacteria, and parasites are 1 source of cancer initiation in humans. Overall, it has been estimated that infectious agents represent 15% to 20% of all cancers in humans (45,46). The International Agency for Research on Cancer has classified at least 11 infectious pathogens as human carcinogens (47). These cancer-causing pathogens include HPV, hepatitis B virus, hepatitis C virus, Epstein-Barr virus, HIV-1, Helicobacter pylori, opisthorchis viverrine, and other agents (38-41,43,44,48). Some of these viruses, their associated cancers, and recommended primary intervention measures are presented in Table 1. These intervention measures can be quantified through health economics research, and the outcomes can help to inform policy decisions. Environmental and Occupational Exposures Environment and occupation are another major exposure factor to cancer-causing carcinogenic substances. The availability of evidence to evaluate the association of specific environmental and occupational exposures and various cancers is very limited, and testing for most chemicals is still incomplete. The International Agency for Research on Cancer and the National Toxicology Program have classified many carcinogenic substances as “sufficient evidence,” indicating a causal relation between exposure to the agent and human cancer, and as “limited evidence,” defined as the observation of a (noncausal) positive association between exposure to the agent and human cancer (49–51). These carcinogenic agents (both sufficient and limited evidence) include specific outdoor and indoor air pollutants, nitrates, pesticides, dioxins, environmental tobacco smoke, certain food additives, benzene, asbestos, solvents, fibers, fine-particle dust (eg, PM2.5), metals, radiation (ionizing and nonionizing), and many other agents. Exposure to these agents may occur on multiple occasions and in various settings during a lifetime, including at workplaces, homes, schools, and entertainment venues. Some of the types of cancers induced by these carcinogens are presented in Table 2. The contributions of these carcinogenic agents to cancer in the United States are substantial. For example, a recent World Health Organization study reported a general estimate that approximately 20% of all cancers are associated with environmental factors and 2% to 10% are associated with occupational exposure (68). These estimates highlight the importance of continued efforts to implement evidence-based primary prevention interventions to prevent these exposures, and health economics research helps to quantify the burden associated with these exposures to inform health policy decisions. Table 2. Selected environmental and occupational carcinogens by risk factors associated with exposure, outcomes, and primary intervention measuresa Exposure factors . Selected risk factors associated with exposureb . Selected outcomes of exposurec . Selected potential primary intervention measures for the exposured . Reference . Environmental carcinogens Nitrates in drinking water Leukemia, bladder, lymphoma, and colorectal cancer Use treatment processes such as installation of ion exchange resin; distillation; reverse osmosis system (52) Motor vehicle exhaust (nitrogen dioxide) Childhood leukemia, central nervous system cancers Reduce outdoor air pollution from motor vehicle traffic by improving infrastructure that supports public transportation, bikeable roads, and other alternatives; use traffic controls that reduce congestion and idling; improve measures to reduce the number of vehicles on the road, such as telecommuting, flexible work hours, and rideshares, and commuting by bicycle (14, 42, 53–55) Indoor air pollutantsb Childhood leukemia and lymphoma cancers Ban of smoking cigarettes in indoor workplaces, public transportation, and indoor public places; reduce burning of wood, incense, or candles and use of gas cooking and heating appliances; reduce workers’ exposure to contaminated air at smokehouses, trash incineration facilities, oil refinery plants, and coal tar and asphalt production plants (53, 56, 57) Environmental organic pollutants (in utero) or POPs Testicular cancer Regulate carcinogenic chemicals such as exposure to pesticides; minimize exposure to POPs through ingestion and inhalation; encourage people of reproductive age to avoid eating large fish, fatty meat, and dairy products that have relatively high levels of POPs and to increase consumption of fibrous foods and green vegetables such as spinach and kale (23, 58) Pesticides such as dioxins Childhood leukemia and lymphoma, brain tumors, germ cell tumors, Hodgkin, NHL Reduce use of pesticides in residential lawns and gardens; reduce direct exposure to pesticides by children; reduce use of pesticides in agricultural products, foods, and drinking water (21, 53) PAHs Lung cancer Encourage people to reduce consumption of smoked and charbroiled foods; avoid exposure to dust, fumes, and skin contact by wearing protective clothing, such as long-sleeve shirts, long pants, and gloves when working with products containing PAHs; eliminate exposure to tobacco smoke; avoid cooking food at very high temperatures and avoid contact of foods with open flames (22) Nitrate consumption Bladder cancer Encourage people to minimize consumption of processed foods and limit meat products such as hot dogs and sausage; eat organic food; eat a diet high in antioxidants (59) Occupational exposures Asbestos Laryngeal, lung, mesothelioma Prohibit use of asbestos in the home and at work; ban export of asbestos; provide asbestos awareness training; provide medical surveillance to workers exposed to asbestos (11, 21) Wood dust Lung, nasal and nasopharynx Encourage or require that workers/supervisors install exhaust ventilation system with collectors placed at points where dust is produced; provide personal protective equipment to reduce wood dust exposure; require wearing of respirators to remove hazardous particulates (dusts) (60) Petroleum products, motor vehicle exhaust (eg, diesel, PAHs, soot, and dioxins) Lung, NHL, soft-tissue sarcoma, skin Increase use of renewable products; perform thermal treatment of waste and clean coal technologies; minimize children’s exposure to toxins (11, 21) Metals (arsenic) Bladder, lung, skin, soft-tissue sarcoma of the liver Reduce exposure to arsenic in food and in safe drinking water and air (53) Reactive chemicals (vinyl chloride) Liver and biliary, soft-tissue sarcoma (angiosarcoma of the liver) Limit chronic or long-term exposure to vinyl chloride; limit use of polyvinyl chloride plastic containers and food packaging; encourage industrial workers in close contact with vinyl chloride to use respirators and wear protective clothing; avoid tobacco smoke (61, 62) Solvents (benzene) Leukemia, NHL Ensure that workers know that if benzene was released indoors, they should go out of the building; if outdoors, should leave the area and move to an area with fresh air; if exposed to benzene, should remove and dispose their clothes, rapidly wash their entire body with soap and water, and get medical care as quickly as possible; practice use of effective personal protective equipment such as breathing protection, helmet with fresh air supply, and face covering operating with positive pressure to blow clean air from inside helmet (47, 63–65) Radiation (ionizing) Bone, brain and central nervous system, breast, leukemia, liver and biliary, lung, multiple myeloma, soft-tissue sarcoma, skin, thyroid Design public policies to avoid unnecessary exposure, including legislation to promote appropriate use of radiological medical procedures; educate physicians to promote use of referral guidelines as decision-making tools to justify diagnostic procedures of choice; educate and train imaging professionals (radiologists and technicians) to apply diagnostic reference levels to radiological procedures to reduce radiation doses without affecting image quality; “Image Wisely”e—encourages imaging providers to limit medical radiation (eg, CT scan, X-rays) in adults; “Image Gently”—elimination of unnecessary testing to minimize radiation in children (63, 66, 67) Radiation (ultraviolet) Skin cancer (basal cell and squamous cell carcinomas) and malignant melanoma Reduce exposure to sun and increase provision of shade in public areas, especially for children and adolescents; encourage people to increase use of sunscreen and avoid using tanning lamps or beds (16, 35) Exposure factors . Selected risk factors associated with exposureb . Selected outcomes of exposurec . Selected potential primary intervention measures for the exposured . Reference . Environmental carcinogens Nitrates in drinking water Leukemia, bladder, lymphoma, and colorectal cancer Use treatment processes such as installation of ion exchange resin; distillation; reverse osmosis system (52) Motor vehicle exhaust (nitrogen dioxide) Childhood leukemia, central nervous system cancers Reduce outdoor air pollution from motor vehicle traffic by improving infrastructure that supports public transportation, bikeable roads, and other alternatives; use traffic controls that reduce congestion and idling; improve measures to reduce the number of vehicles on the road, such as telecommuting, flexible work hours, and rideshares, and commuting by bicycle (14, 42, 53–55) Indoor air pollutantsb Childhood leukemia and lymphoma cancers Ban of smoking cigarettes in indoor workplaces, public transportation, and indoor public places; reduce burning of wood, incense, or candles and use of gas cooking and heating appliances; reduce workers’ exposure to contaminated air at smokehouses, trash incineration facilities, oil refinery plants, and coal tar and asphalt production plants (53, 56, 57) Environmental organic pollutants (in utero) or POPs Testicular cancer Regulate carcinogenic chemicals such as exposure to pesticides; minimize exposure to POPs through ingestion and inhalation; encourage people of reproductive age to avoid eating large fish, fatty meat, and dairy products that have relatively high levels of POPs and to increase consumption of fibrous foods and green vegetables such as spinach and kale (23, 58) Pesticides such as dioxins Childhood leukemia and lymphoma, brain tumors, germ cell tumors, Hodgkin, NHL Reduce use of pesticides in residential lawns and gardens; reduce direct exposure to pesticides by children; reduce use of pesticides in agricultural products, foods, and drinking water (21, 53) PAHs Lung cancer Encourage people to reduce consumption of smoked and charbroiled foods; avoid exposure to dust, fumes, and skin contact by wearing protective clothing, such as long-sleeve shirts, long pants, and gloves when working with products containing PAHs; eliminate exposure to tobacco smoke; avoid cooking food at very high temperatures and avoid contact of foods with open flames (22) Nitrate consumption Bladder cancer Encourage people to minimize consumption of processed foods and limit meat products such as hot dogs and sausage; eat organic food; eat a diet high in antioxidants (59) Occupational exposures Asbestos Laryngeal, lung, mesothelioma Prohibit use of asbestos in the home and at work; ban export of asbestos; provide asbestos awareness training; provide medical surveillance to workers exposed to asbestos (11, 21) Wood dust Lung, nasal and nasopharynx Encourage or require that workers/supervisors install exhaust ventilation system with collectors placed at points where dust is produced; provide personal protective equipment to reduce wood dust exposure; require wearing of respirators to remove hazardous particulates (dusts) (60) Petroleum products, motor vehicle exhaust (eg, diesel, PAHs, soot, and dioxins) Lung, NHL, soft-tissue sarcoma, skin Increase use of renewable products; perform thermal treatment of waste and clean coal technologies; minimize children’s exposure to toxins (11, 21) Metals (arsenic) Bladder, lung, skin, soft-tissue sarcoma of the liver Reduce exposure to arsenic in food and in safe drinking water and air (53) Reactive chemicals (vinyl chloride) Liver and biliary, soft-tissue sarcoma (angiosarcoma of the liver) Limit chronic or long-term exposure to vinyl chloride; limit use of polyvinyl chloride plastic containers and food packaging; encourage industrial workers in close contact with vinyl chloride to use respirators and wear protective clothing; avoid tobacco smoke (61, 62) Solvents (benzene) Leukemia, NHL Ensure that workers know that if benzene was released indoors, they should go out of the building; if outdoors, should leave the area and move to an area with fresh air; if exposed to benzene, should remove and dispose their clothes, rapidly wash their entire body with soap and water, and get medical care as quickly as possible; practice use of effective personal protective equipment such as breathing protection, helmet with fresh air supply, and face covering operating with positive pressure to blow clean air from inside helmet (47, 63–65) Radiation (ionizing) Bone, brain and central nervous system, breast, leukemia, liver and biliary, lung, multiple myeloma, soft-tissue sarcoma, skin, thyroid Design public policies to avoid unnecessary exposure, including legislation to promote appropriate use of radiological medical procedures; educate physicians to promote use of referral guidelines as decision-making tools to justify diagnostic procedures of choice; educate and train imaging professionals (radiologists and technicians) to apply diagnostic reference levels to radiological procedures to reduce radiation doses without affecting image quality; “Image Wisely”e—encourages imaging providers to limit medical radiation (eg, CT scan, X-rays) in adults; “Image Gently”—elimination of unnecessary testing to minimize radiation in children (63, 66, 67) Radiation (ultraviolet) Skin cancer (basal cell and squamous cell carcinomas) and malignant melanoma Reduce exposure to sun and increase provision of shade in public areas, especially for children and adolescents; encourage people to increase use of sunscreen and avoid using tanning lamps or beds (16, 35) a Source: authors’ compilation. This table provided more details on one of the exposure factors (environmental and occupational) presented in the figure. NHL = non-Hodgkin’s lymphoma; PAH = poly-aromatic hydrocarbon; POP = persistent organic pollutant. b Selected risk factors associated with exposure (carcinogenic agent) based on a Group 1 designation by the International Agency for Research on Cancer (44, 49, 50). c Selected outcomes of the exposure are those classified as “strong evidence” of causal link to the carcinogenic agent based on a Group 1 designation by the International Agency for Research on Cancer (44, 49, 50). d The effectiveness and economic impact of some of these environmental and occupational primary prevention measures have not been quantified. This is partly due to lack of data. With data, health economics research can help quantify their economic benefits. e Image Wisely encourages imaging providers to 1) optimize use of radiation to use only the radiation necessary to produce diagnostic quality images; 2) convey the principles of the Image Wisely initiative to the imaging team to ensure that the facility optimizes its use of radiation when imaging patients; 3) communicate optimal patient imaging strategies to referring physicians and be available for consultation; and 4) routinely review imaging protocols to ensure the use of the least amount of radiation necessary to acquire a quality diagnostic image (63, 67). Open in new tab Table 2. Selected environmental and occupational carcinogens by risk factors associated with exposure, outcomes, and primary intervention measuresa Exposure factors . Selected risk factors associated with exposureb . Selected outcomes of exposurec . Selected potential primary intervention measures for the exposured . Reference . Environmental carcinogens Nitrates in drinking water Leukemia, bladder, lymphoma, and colorectal cancer Use treatment processes such as installation of ion exchange resin; distillation; reverse osmosis system (52) Motor vehicle exhaust (nitrogen dioxide) Childhood leukemia, central nervous system cancers Reduce outdoor air pollution from motor vehicle traffic by improving infrastructure that supports public transportation, bikeable roads, and other alternatives; use traffic controls that reduce congestion and idling; improve measures to reduce the number of vehicles on the road, such as telecommuting, flexible work hours, and rideshares, and commuting by bicycle (14, 42, 53–55) Indoor air pollutantsb Childhood leukemia and lymphoma cancers Ban of smoking cigarettes in indoor workplaces, public transportation, and indoor public places; reduce burning of wood, incense, or candles and use of gas cooking and heating appliances; reduce workers’ exposure to contaminated air at smokehouses, trash incineration facilities, oil refinery plants, and coal tar and asphalt production plants (53, 56, 57) Environmental organic pollutants (in utero) or POPs Testicular cancer Regulate carcinogenic chemicals such as exposure to pesticides; minimize exposure to POPs through ingestion and inhalation; encourage people of reproductive age to avoid eating large fish, fatty meat, and dairy products that have relatively high levels of POPs and to increase consumption of fibrous foods and green vegetables such as spinach and kale (23, 58) Pesticides such as dioxins Childhood leukemia and lymphoma, brain tumors, germ cell tumors, Hodgkin, NHL Reduce use of pesticides in residential lawns and gardens; reduce direct exposure to pesticides by children; reduce use of pesticides in agricultural products, foods, and drinking water (21, 53) PAHs Lung cancer Encourage people to reduce consumption of smoked and charbroiled foods; avoid exposure to dust, fumes, and skin contact by wearing protective clothing, such as long-sleeve shirts, long pants, and gloves when working with products containing PAHs; eliminate exposure to tobacco smoke; avoid cooking food at very high temperatures and avoid contact of foods with open flames (22) Nitrate consumption Bladder cancer Encourage people to minimize consumption of processed foods and limit meat products such as hot dogs and sausage; eat organic food; eat a diet high in antioxidants (59) Occupational exposures Asbestos Laryngeal, lung, mesothelioma Prohibit use of asbestos in the home and at work; ban export of asbestos; provide asbestos awareness training; provide medical surveillance to workers exposed to asbestos (11, 21) Wood dust Lung, nasal and nasopharynx Encourage or require that workers/supervisors install exhaust ventilation system with collectors placed at points where dust is produced; provide personal protective equipment to reduce wood dust exposure; require wearing of respirators to remove hazardous particulates (dusts) (60) Petroleum products, motor vehicle exhaust (eg, diesel, PAHs, soot, and dioxins) Lung, NHL, soft-tissue sarcoma, skin Increase use of renewable products; perform thermal treatment of waste and clean coal technologies; minimize children’s exposure to toxins (11, 21) Metals (arsenic) Bladder, lung, skin, soft-tissue sarcoma of the liver Reduce exposure to arsenic in food and in safe drinking water and air (53) Reactive chemicals (vinyl chloride) Liver and biliary, soft-tissue sarcoma (angiosarcoma of the liver) Limit chronic or long-term exposure to vinyl chloride; limit use of polyvinyl chloride plastic containers and food packaging; encourage industrial workers in close contact with vinyl chloride to use respirators and wear protective clothing; avoid tobacco smoke (61, 62) Solvents (benzene) Leukemia, NHL Ensure that workers know that if benzene was released indoors, they should go out of the building; if outdoors, should leave the area and move to an area with fresh air; if exposed to benzene, should remove and dispose their clothes, rapidly wash their entire body with soap and water, and get medical care as quickly as possible; practice use of effective personal protective equipment such as breathing protection, helmet with fresh air supply, and face covering operating with positive pressure to blow clean air from inside helmet (47, 63–65) Radiation (ionizing) Bone, brain and central nervous system, breast, leukemia, liver and biliary, lung, multiple myeloma, soft-tissue sarcoma, skin, thyroid Design public policies to avoid unnecessary exposure, including legislation to promote appropriate use of radiological medical procedures; educate physicians to promote use of referral guidelines as decision-making tools to justify diagnostic procedures of choice; educate and train imaging professionals (radiologists and technicians) to apply diagnostic reference levels to radiological procedures to reduce radiation doses without affecting image quality; “Image Wisely”e—encourages imaging providers to limit medical radiation (eg, CT scan, X-rays) in adults; “Image Gently”—elimination of unnecessary testing to minimize radiation in children (63, 66, 67) Radiation (ultraviolet) Skin cancer (basal cell and squamous cell carcinomas) and malignant melanoma Reduce exposure to sun and increase provision of shade in public areas, especially for children and adolescents; encourage people to increase use of sunscreen and avoid using tanning lamps or beds (16, 35) Exposure factors . Selected risk factors associated with exposureb . Selected outcomes of exposurec . Selected potential primary intervention measures for the exposured . Reference . Environmental carcinogens Nitrates in drinking water Leukemia, bladder, lymphoma, and colorectal cancer Use treatment processes such as installation of ion exchange resin; distillation; reverse osmosis system (52) Motor vehicle exhaust (nitrogen dioxide) Childhood leukemia, central nervous system cancers Reduce outdoor air pollution from motor vehicle traffic by improving infrastructure that supports public transportation, bikeable roads, and other alternatives; use traffic controls that reduce congestion and idling; improve measures to reduce the number of vehicles on the road, such as telecommuting, flexible work hours, and rideshares, and commuting by bicycle (14, 42, 53–55) Indoor air pollutantsb Childhood leukemia and lymphoma cancers Ban of smoking cigarettes in indoor workplaces, public transportation, and indoor public places; reduce burning of wood, incense, or candles and use of gas cooking and heating appliances; reduce workers’ exposure to contaminated air at smokehouses, trash incineration facilities, oil refinery plants, and coal tar and asphalt production plants (53, 56, 57) Environmental organic pollutants (in utero) or POPs Testicular cancer Regulate carcinogenic chemicals such as exposure to pesticides; minimize exposure to POPs through ingestion and inhalation; encourage people of reproductive age to avoid eating large fish, fatty meat, and dairy products that have relatively high levels of POPs and to increase consumption of fibrous foods and green vegetables such as spinach and kale (23, 58) Pesticides such as dioxins Childhood leukemia and lymphoma, brain tumors, germ cell tumors, Hodgkin, NHL Reduce use of pesticides in residential lawns and gardens; reduce direct exposure to pesticides by children; reduce use of pesticides in agricultural products, foods, and drinking water (21, 53) PAHs Lung cancer Encourage people to reduce consumption of smoked and charbroiled foods; avoid exposure to dust, fumes, and skin contact by wearing protective clothing, such as long-sleeve shirts, long pants, and gloves when working with products containing PAHs; eliminate exposure to tobacco smoke; avoid cooking food at very high temperatures and avoid contact of foods with open flames (22) Nitrate consumption Bladder cancer Encourage people to minimize consumption of processed foods and limit meat products such as hot dogs and sausage; eat organic food; eat a diet high in antioxidants (59) Occupational exposures Asbestos Laryngeal, lung, mesothelioma Prohibit use of asbestos in the home and at work; ban export of asbestos; provide asbestos awareness training; provide medical surveillance to workers exposed to asbestos (11, 21) Wood dust Lung, nasal and nasopharynx Encourage or require that workers/supervisors install exhaust ventilation system with collectors placed at points where dust is produced; provide personal protective equipment to reduce wood dust exposure; require wearing of respirators to remove hazardous particulates (dusts) (60) Petroleum products, motor vehicle exhaust (eg, diesel, PAHs, soot, and dioxins) Lung, NHL, soft-tissue sarcoma, skin Increase use of renewable products; perform thermal treatment of waste and clean coal technologies; minimize children’s exposure to toxins (11, 21) Metals (arsenic) Bladder, lung, skin, soft-tissue sarcoma of the liver Reduce exposure to arsenic in food and in safe drinking water and air (53) Reactive chemicals (vinyl chloride) Liver and biliary, soft-tissue sarcoma (angiosarcoma of the liver) Limit chronic or long-term exposure to vinyl chloride; limit use of polyvinyl chloride plastic containers and food packaging; encourage industrial workers in close contact with vinyl chloride to use respirators and wear protective clothing; avoid tobacco smoke (61, 62) Solvents (benzene) Leukemia, NHL Ensure that workers know that if benzene was released indoors, they should go out of the building; if outdoors, should leave the area and move to an area with fresh air; if exposed to benzene, should remove and dispose their clothes, rapidly wash their entire body with soap and water, and get medical care as quickly as possible; practice use of effective personal protective equipment such as breathing protection, helmet with fresh air supply, and face covering operating with positive pressure to blow clean air from inside helmet (47, 63–65) Radiation (ionizing) Bone, brain and central nervous system, breast, leukemia, liver and biliary, lung, multiple myeloma, soft-tissue sarcoma, skin, thyroid Design public policies to avoid unnecessary exposure, including legislation to promote appropriate use of radiological medical procedures; educate physicians to promote use of referral guidelines as decision-making tools to justify diagnostic procedures of choice; educate and train imaging professionals (radiologists and technicians) to apply diagnostic reference levels to radiological procedures to reduce radiation doses without affecting image quality; “Image Wisely”e—encourages imaging providers to limit medical radiation (eg, CT scan, X-rays) in adults; “Image Gently”—elimination of unnecessary testing to minimize radiation in children (63, 66, 67) Radiation (ultraviolet) Skin cancer (basal cell and squamous cell carcinomas) and malignant melanoma Reduce exposure to sun and increase provision of shade in public areas, especially for children and adolescents; encourage people to increase use of sunscreen and avoid using tanning lamps or beds (16, 35) a Source: authors’ compilation. This table provided more details on one of the exposure factors (environmental and occupational) presented in the figure. NHL = non-Hodgkin’s lymphoma; PAH = poly-aromatic hydrocarbon; POP = persistent organic pollutant. b Selected risk factors associated with exposure (carcinogenic agent) based on a Group 1 designation by the International Agency for Research on Cancer (44, 49, 50). c Selected outcomes of the exposure are those classified as “strong evidence” of causal link to the carcinogenic agent based on a Group 1 designation by the International Agency for Research on Cancer (44, 49, 50). d The effectiveness and economic impact of some of these environmental and occupational primary prevention measures have not been quantified. This is partly due to lack of data. With data, health economics research can help quantify their economic benefits. e Image Wisely encourages imaging providers to 1) optimize use of radiation to use only the radiation necessary to produce diagnostic quality images; 2) convey the principles of the Image Wisely initiative to the imaging team to ensure that the facility optimizes its use of radiation when imaging patients; 3) communicate optimal patient imaging strategies to referring physicians and be available for consultation; and 4) routinely review imaging protocols to ensure the use of the least amount of radiation necessary to acquire a quality diagnostic image (63, 67). Open in new tab Behavioral Factors Like environmental and occupational determinants of cancer, behavioral factors also substantially contribute to the initiation and progression of cancer in humans. Examples of some of the cancers caused by behavioral factors and their recommended interventions are presented in Table 3. These behavioral factors include tobacco use, alcohol consumption, diet, nutrition, and physical activity. For decades, it has been well established that cigarette smoking causes several types of cancer (15,69,70,79), and it is associated with approximately 25% to 30% of all cancer deaths (20,28,29). Among these cancers, smoking accounts for approximately 90% of lung cancer deaths (12,28). Additionally, it has been documented that nonsmokers who are exposed to secondhand smoke have an elevated risk of being diagnosed with lung cancer (13). Like tobacco use, alcohol consumption is also a well-established modifiable risk for many cancers (71,80). Similarly, based on information from the Continuous Update Project Panel and other studies, unhealthy diet, lack of physical activity, and other sedentary behaviors contributed to increased overweight and obesity, which are associated with many types of cancer (12,74,77). It is worth noting that a few studies have reported harmful impact on health due to deliberate weight loss for people who are overweight with a body mass index of 35 kg/m2 or less (81). On the other hand, there is consistent evidence that a high body mass index is associated with increased risks of at least 13 types of cancer, and these cancers make up 40% of all cancers diagnosed in the United States each year (77). The risk of cancer associated with behavioral factors can be reduced with many available and recommended primary prevention interventions, as presented in Table 3. These primary intervention measures can be quantified through health economics research, and the outcomes can be used as inputs to inform policy decisions. Table 3. Selected behavioral risk factors and related chronic conditions by outcomes and primary intervention measuresa,b Risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for reduce outcomes of exposure . Reference . Tobacco and smoking Lung, liver, bladder, larynx, renal parenchyma, penis, oropharynx, oropharyngeal, anus, renal pelvis, stomach, uterus, pancreas, vulva, cervical Prevent people from starting to smoke; increase combustible tobacco prices; pass comprehensive smoke-free laws; conduct antitobacco mass media campaigns; promote barrier-free access to tobacco cessation counseling and treatment; eliminate exposure to secondhand smoke (15, 69, 70) Alcohol use Stomach, colorectal, oropharynx, liver, breast (postmenopause), oesophagus (squamous cell carcinoma), larynx Screen for excessive alcohol use; increase tobacco prices; regulate concentration of alcohol retailers in an area; enhance enforcement of laws prohibiting alcohol sales to minors (<21 y); provide behavioral counseling to reduce misuse (71–73) Poor diet and nutrition Lung, colorectal, pancreas, prostate, gallbladder, esophagus, gastric, breast, endometrial, larynx, mouth, pharynx Encourage people to limit calorie-dense meals; limit sugar-sweetened beverages; reduce intake of red meat; avoid processed meats; consume diet rich in whole grains, legumes, vegetables, fruits, and spices (74–76) Overweight and obesity Colorectal, multiple myeloma, kidney, esophageal (adenocarcinoma), liver, breast (postmenopause), pancreatic, ovarian, non-Hodgkin’s lymphoma, gallbladder, upper stomach, uterine, endometrial, meningioma, thyroid Support healthy eating and active living in variety of settings: communities, worksites, schools, and early care and education facilities; encourage people to eat a healthy diet and engage in sufficient physical activity; maintain healthy weight throughout life, and reduce intake of sugar sweetened drinks (77, 78) Risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for reduce outcomes of exposure . Reference . Tobacco and smoking Lung, liver, bladder, larynx, renal parenchyma, penis, oropharynx, oropharyngeal, anus, renal pelvis, stomach, uterus, pancreas, vulva, cervical Prevent people from starting to smoke; increase combustible tobacco prices; pass comprehensive smoke-free laws; conduct antitobacco mass media campaigns; promote barrier-free access to tobacco cessation counseling and treatment; eliminate exposure to secondhand smoke (15, 69, 70) Alcohol use Stomach, colorectal, oropharynx, liver, breast (postmenopause), oesophagus (squamous cell carcinoma), larynx Screen for excessive alcohol use; increase tobacco prices; regulate concentration of alcohol retailers in an area; enhance enforcement of laws prohibiting alcohol sales to minors (<21 y); provide behavioral counseling to reduce misuse (71–73) Poor diet and nutrition Lung, colorectal, pancreas, prostate, gallbladder, esophagus, gastric, breast, endometrial, larynx, mouth, pharynx Encourage people to limit calorie-dense meals; limit sugar-sweetened beverages; reduce intake of red meat; avoid processed meats; consume diet rich in whole grains, legumes, vegetables, fruits, and spices (74–76) Overweight and obesity Colorectal, multiple myeloma, kidney, esophageal (adenocarcinoma), liver, breast (postmenopause), pancreatic, ovarian, non-Hodgkin’s lymphoma, gallbladder, upper stomach, uterine, endometrial, meningioma, thyroid Support healthy eating and active living in variety of settings: communities, worksites, schools, and early care and education facilities; encourage people to eat a healthy diet and engage in sufficient physical activity; maintain healthy weight throughout life, and reduce intake of sugar sweetened drinks (77, 78) a Source: authors’ compilation. b This table provides more details on one of the exposure factors (behavioral) presented in Figure 1. The potential primary intervention measures included in the table can be quantified through health economics research. Open in new tab Table 3. Selected behavioral risk factors and related chronic conditions by outcomes and primary intervention measuresa,b Risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for reduce outcomes of exposure . Reference . Tobacco and smoking Lung, liver, bladder, larynx, renal parenchyma, penis, oropharynx, oropharyngeal, anus, renal pelvis, stomach, uterus, pancreas, vulva, cervical Prevent people from starting to smoke; increase combustible tobacco prices; pass comprehensive smoke-free laws; conduct antitobacco mass media campaigns; promote barrier-free access to tobacco cessation counseling and treatment; eliminate exposure to secondhand smoke (15, 69, 70) Alcohol use Stomach, colorectal, oropharynx, liver, breast (postmenopause), oesophagus (squamous cell carcinoma), larynx Screen for excessive alcohol use; increase tobacco prices; regulate concentration of alcohol retailers in an area; enhance enforcement of laws prohibiting alcohol sales to minors (<21 y); provide behavioral counseling to reduce misuse (71–73) Poor diet and nutrition Lung, colorectal, pancreas, prostate, gallbladder, esophagus, gastric, breast, endometrial, larynx, mouth, pharynx Encourage people to limit calorie-dense meals; limit sugar-sweetened beverages; reduce intake of red meat; avoid processed meats; consume diet rich in whole grains, legumes, vegetables, fruits, and spices (74–76) Overweight and obesity Colorectal, multiple myeloma, kidney, esophageal (adenocarcinoma), liver, breast (postmenopause), pancreatic, ovarian, non-Hodgkin’s lymphoma, gallbladder, upper stomach, uterine, endometrial, meningioma, thyroid Support healthy eating and active living in variety of settings: communities, worksites, schools, and early care and education facilities; encourage people to eat a healthy diet and engage in sufficient physical activity; maintain healthy weight throughout life, and reduce intake of sugar sweetened drinks (77, 78) Risk factors associated with exposure (carcinogenic agent) . Selected outcomes of exposure . Selected primary intervention measures for reduce outcomes of exposure . Reference . Tobacco and smoking Lung, liver, bladder, larynx, renal parenchyma, penis, oropharynx, oropharyngeal, anus, renal pelvis, stomach, uterus, pancreas, vulva, cervical Prevent people from starting to smoke; increase combustible tobacco prices; pass comprehensive smoke-free laws; conduct antitobacco mass media campaigns; promote barrier-free access to tobacco cessation counseling and treatment; eliminate exposure to secondhand smoke (15, 69, 70) Alcohol use Stomach, colorectal, oropharynx, liver, breast (postmenopause), oesophagus (squamous cell carcinoma), larynx Screen for excessive alcohol use; increase tobacco prices; regulate concentration of alcohol retailers in an area; enhance enforcement of laws prohibiting alcohol sales to minors (<21 y); provide behavioral counseling to reduce misuse (71–73) Poor diet and nutrition Lung, colorectal, pancreas, prostate, gallbladder, esophagus, gastric, breast, endometrial, larynx, mouth, pharynx Encourage people to limit calorie-dense meals; limit sugar-sweetened beverages; reduce intake of red meat; avoid processed meats; consume diet rich in whole grains, legumes, vegetables, fruits, and spices (74–76) Overweight and obesity Colorectal, multiple myeloma, kidney, esophageal (adenocarcinoma), liver, breast (postmenopause), pancreatic, ovarian, non-Hodgkin’s lymphoma, gallbladder, upper stomach, uterine, endometrial, meningioma, thyroid Support healthy eating and active living in variety of settings: communities, worksites, schools, and early care and education facilities; encourage people to eat a healthy diet and engage in sufficient physical activity; maintain healthy weight throughout life, and reduce intake of sugar sweetened drinks (77, 78) a Source: authors’ compilation. b This table provides more details on one of the exposure factors (behavioral) presented in Figure 1. The potential primary intervention measures included in the table can be quantified through health economics research. Open in new tab Description of Existing Primary Prevention Interventions for Each Exposure Factor to Reduce the Incidence of Cancer Because of the complex process in which cancer develops in humans, it may be impossible to know the full range of agents or combination of agents that can cause cancer. However, it is well documented that the majority of exposures associated with initiation and development of cancers in humans are preventable (13,15,68). A study by DeVita et al. (15) chronicled important events in the past 200 years in cancer prevention. These events include progress in chemoprevention and in discoveries of interactions between infectious agents and cancer as well as discoveries of the impact of tobacco use in cancer disease. Based on these discoveries, advances in environmental and occupational health research, and a better understanding of the factors that influence behavioral choices in the past decades, there are many evidence-based recommendations to eliminate or reduce the presence, use, or consumption of cancer-causing carcinogenic agents (16,33,35,36,39,42,44,48,58,70–72,78,82). These recommendations have been promulgated by entities such as the US Preventive Services Task Force, the Advisory Committee on Immunizations Practices, the Food and Drug Administration, the Environmental Protection Agency, the Community Preventive Services Task Force (CPSTF), and the World Cancer Research Fund/American Institute for Cancer Research (16,33,35,36,39,42,44,48,58,70–72,74,78,82). The preventive interventions recommended by these organizations have proven to be an essential aspect of disease prevention and health promotion in the US, but they are consistently underused (83,84). According to the US Preventive Services Task Force, genetic counseling and testing are recommended for individuals at increased risk of certain cancers associated with inherited genetic mutations (33–35). The recommendations requires that counseling include a full explanation of the risks and benefits of genetic testing, informed consent, and psychosocial issues that may extend beyond those encountered in a general oncology office (33–35). An increase in the proportion of females at higher risk of breast or ovarian cancer who receive genetic counseling is one of the Healthy People 2030 developmental objectives on cancer preventive care (85). For cancers caused by infectious agents, the recommended set of primary prevention interventions includes prophylactic vaccines for preventing HPV and hepatitis B virus (38,40–42) and treatment for H. pylori, hepatitis C virus, HIV, and other cancer-causing infections (39,43,44). Many primary prevention interventions shown to be effective in eliminating or decreasing exposure to environmental and occupational carcinogens have been identified. Many of these interventions are listed in the World Health Organization’s “Primary prevention of cancer through mitigation of environmental and occupational determinants” (86). Similarly, a systematic study by Espina et al. (87) presented an evidence-based global strategy for the primary prevention of environmental and occupational cancers. The economic impact of some of these environmental and occupational prevention measures in reducing the initiation and progression of cancer has not been quantified (Table 2). Primary interventions to eliminate or reduce the harmful impact of behavioral factors, including tobacco use, alcohol consumption, unhealthy diet, and physical inactivity, that are associated with the initiation of cancer have been discussed by multiple organizations and investigators (Table 3) (71,72,88). Some of these preventive interventions involve direct economic activities, such as increasing the price of alcohol, sugar-sweetened beverages, or combustible tobacco, often through excise taxes (70–72). Other interventions have indirect economic effects, such as creating barriers to access to alcohol, combustible tobacco, or foods low in nutritional value, or, conversely, increasing access to affordable, healthy foods and environments for physical activity (70–72,74,75,78). Although the effectiveness of many primary prevention interventions has been documented, more information about their economic evidence to inform both the short- and long-term resource allocation decisions to reduce cancer incidence is needed. Gaps and Unmet Needs in Health Economics Research Focused on Primary Prevention of Cancer Although primary prevention can be an effective and cost-effective approach for reducing the risk of cancers caused by exposures described earlier, multiple knowledge gaps regarding factors affecting the economics of primary prevention of cancer remain. For example, primary prevention interventions may occur years (or decades) before a targeted population is at the highest risk of developing cancer associated with the prevented activities or risk factors. Collecting robust data linking primary prevention interventions and subsequent cancer incidence is therefore extremely challenging and may be expensive. More research could help link short- and intermediate-term changes in risk factors and health outcomes from prevention interventions to longer-term outcomes and increase the use of modeling to better project primary intervention effects. In addition to documenting outcomes from prevention interventions, the costs of conducting primary prevention interventions are also often not well documented. When such costs are assessed, they may be based on rough estimates from salaries of intervention personnel and supplies used rather than on more detailed assessments of the value of all the resources required to deliver the intervention. Cancer health economics researchers may want to partner with implementation scientists to better assess the processes and associated costs for implementing and disseminating interventions that have been shown to be effective in pilot studies. For example, in the CPSTF recommendations, health economists regularly work with epidemiologists and medical officers to quantify the cost-effectiveness of prevention interventions that have been found to be effective (89,90). This type of collaborative work could support primary prevention of cancer interventions. One critical gap is that many policy interventions to prevent cancer are understudied in the United States because it is not possible to link policy exposure to survey or administrative data that could help to evaluate both intended and unintended effects of the intervention. For instance, the link between how disparities in cancer risk factors translate into economic and health disparities in the population is understudied. Geocodes may be needed for these linkages but may not be available because of concerns over patient confidentiality. One potential option would be to provide publicly available data aggregated by geography (eg, state), which would be enough to permit many policy intervention studies without compromising data security. In addition, some of the critical information needed to analyze the economics of primary prevention of cancer interventions may not be available. This may include details regarding the delivery of the primary prevention interventions, the motivations participants have for engaging in these interventions, the costs participants incur (eg, transportation, parking, childcare), and the impact of interventions on health-related beliefs and behaviors. Such gaps in information are even more problematic when attempting to evaluate the economics of prevention-focused cancer interventions among underserved populations. Medically underserved individuals may be underrepresented in available data resources, and their care may be even more fragmented. Further, social determinants of health (SDoH) may have particularly important effects on the economics of cancer prevention for individuals from racial and ethnic minority groups, people with lower incomes, people who live in rural areas, and other populations at increased risk for cancer, but information on SDoH may be incomplete or missing from available data. Better collection of standardized SDoH data and data on social needs and social risk factors could help address these gaps in the future. With enhanced collection of standardized SDoH data, health economics researchers can develop models to better project associations between socioeconomics determinants (inequalities and inequities) and potential interventions for the primary prevention of cancer. These models can then be used to tailor interventions to improve the effectiveness and cost-effectiveness of interventions for the primary prevention of cancer among populations that are medically underserved or at higher risk of cancer. In addition, programs can be developed to improve daily living conditions, tackle unequal distribution of resources, and estimate the cost vs benefit of interventions for the primary prevention of cancer (eg, education vs taxation targeting excess alcohol consumption) in different communities. An additional unmet need in prevention-focused cancer health economics research is timely involvement of community-based organizations. Many existing prevention interventions require community engagement for participant recruitment, intervention delivery, and accurate follow-up. However, some researchers may not engage community leaders or community-based organizations early in the development of intervention plans, potentially compromising cost-effectiveness as well as potential relevance or usefulness to the intended recipients, while also potentially restricting the population that can receive the intervention. Similarly, the development of important collaborations between cancer health economics researchers and community-based advocates or policy makers interested in cancer prevention may be of benefit. Researchers may need to learn to communicate with nonresearcher audiences to help address these unmet needs. Training is also an important unmet need for health economics research focused on cancer prevention. Efforts could be made to improve training among both undergraduate and graduate students as well as among clinical trainees. This includes interdisciplinary or cross-disciplinary training, bringing together economists, health services researchers, decision scientists, epidemiologists, statisticians, clinicians, and others. Training could be enhanced through collaborations between economics departments, schools and programs of public health, medical schools, public health agencies, and other allied health departments. Because primary prevention intervention research involves a community focus, it is therefore critical that this training also involve a community focus. Such training can include partnerships with community-based organizations and advocates, policy makers, and government officials, and provide experience in community-based participatory research. In addition to helping advance the field of cancer health economics research and address the challenges of studying primary prevention, improving training opportunities could help research professionals learn new methods and develop new approaches. The 1971 National Cancer Act contributed to the growth and evolution of health economics research in NCI. A few studies in this special supplement provided information on the history and funding of health economics research in NCI (90,91). However, many important aspects in economics of primary prevention of cancer have not been addressed through NCI funding. Funding opportunity announcements or notice of special interests could be further developed to foster more research in health economics. Because health economics methods vary considerably across subspecialties, study section reviewers need to be carefully chosen. For example, a health economist with expertise in natural experiments may not be an appropriate reviewer for a cost-effectiveness study and vice versa. Collaborations between individuals from diverse disciplines should be encouraged because cancer health economics research is a transdisciplinary field. These collaborations can draw on knowledge from “team science” by bringing together researchers who may not share common methods, scientific approaches, or even research vocabularies (92). In addition, efforts to enhance dissemination of health economics research findings on primary prevention would be valuable to nonresearcher audiences such as policy makers and community leaders, who are often key for gaining widespread interest and engagement in cancer prevention activities. Additionally, knowledge translation of economic research for communication to advocates, health practitioners, decision makers, and the target population is also underserved. Challenges in Conducting Health Economics Research Focused on Primary Prevention of Cancer The outcome of prevention is not immediate (17). This is a challenge most health economists conducting health economics research on primary prevention of cancer know too well. Cancer as a disease develops slowly, so it takes years or decades to observe the impact of primary intervention efforts. As such, the benefits of the intervention may become difficult to be accounted for and to be credited to the payer of the prevention. Further, primary prevention guidelines are constantly changing and in some cases are inconsistent. For example, some guidelines provide limits for moderate alcohol consumption, whereas others report that any amount of alcohol use is harmful to human health (93). Activities to reduce the development of cancer can continue throughout the lifespan (10,18). Also, some aspects of primary prevention may be expensive; even when primary prevention is inexpensive (or free), individuals may have personal conflicts such as religious or cultural beliefs that restrict them from participating in an intervention. Based on these and other impediments, it is often challenging to estimate the true economic costs and benefits of primary prevention of cancer. Other challenges faced by health economics researchers is the reliance on quasi- or natural experimental study designs to establish a causal link between health outcome and primary prevention interventions. However, natural experiments involving cancer are often infrequent and potentially of limited generalizability. Hence, researchers use observational studies based on existing databases that may have dated information and are inadequate to convert health outcomes into policy recommendations that can be implemented to improve population health. A related challenge is data accessibility. Individuals may receive cancer-focused preventive care (eg, HPV or hepatitis B vaccination, smoking prevention, or cessation interventions, etc) through 1 health-care system or while covered by 1 type of health insurance. They will likely see health-care providers affiliated with multiple other health-care systems and be covered by other types of health insurance throughout their lives. Being able to access these fragmented pieces of health information about individuals could be a substantial barrier to conducting cancer health economics research focused on primary prevention. Even when more comprehensive data are available, for example, from an all-payer claims data resource, the cost of accessing such data may be prohibitive. As previously described, geographic data are also needed to conduct natural experiment–style studies of policy changes. Because of the issues highlighted above, in general, primary prevention of cancer may not be fully accepted in the private sector for commercial interests. The business case for primary prevention of cancer interventions is different from that related to cancer screening, treatment, and survivorship care. Opportunities in Health Economics Research Focused on Primary Prevention of Cancer Amid the challenges in conducting health economics research on primary prevention of cancer, there are also many opportunities, which may be classified into 2 broad approaches: economic evaluation and applied micro-econometric research. Within these 2 broad areas, there are many methods and approaches economists have used over the years to estimate the costs and benefits of primary prevention of cancer. Some of these methods and approaches are discussed below. Economic Evaluation Economic evaluations require consideration of the costs and consequences of various interventions for cancer prevention. The method includes cost-effectiveness analysis, cost-utility analysis, and cost-benefit analysis, and all are well recognized and have been used to quantify the benefits of primary prevention of cancer interventions (90,94). Using these methods, health economists have an opportunity to provide inputs that decision makers can consider to effectively allocate health prevention resources based on many factors that may include individual or group preference. For example, outcomes from health economic evaluations can reveal that some population groups are more likely to have occupations that put them at increased risk of exposure to carcinogenic agents. This outcome may be one of the inputs that decision makers would consider in allocating prevention resources to different segments of the population. Further, as an area of growing interest, economists have an opportunity to work with clinicians in adding an economic component to randomized clinical trials that can provide timely data on both costs and health outcomes. The data can be used as part of the input to evaluate the costs and benefits of the trials to the population being studied. Similarly, as the CPSTF has begun to incorporate economic evaluation information into the development of their respective evidence-based recommendations for health services (89,90), health economists have an opportunity to help interpret the economic data in these guidelines to decision makers at all levels. The ability to use the available cancer registry data (95) is an important opportunity for economic evaluations of cancer prevention. The registry data, combined with sophisticated decision analysis models, can allow for rigorous estimates of the effect of primary cancer interventions on short- and long-term outcomes (Figure 1). Applied Micro-Econometric Research In past decades, advances in data science and economic methods have offered exciting new opportunities in applied micro-econometric health economics research in primary prevention of cancer (96,97). This approach provides evidence about the causal relationships between specific cancer risk factors and outcomes. It can also allow causal inferences about the links between primary prevention of cancer, public policies, and SDoH. For example, micro-econometric research could estimate whether policies that regulate alcohol retail stores in an area (eg, neighborhood or city) could reduce alcohol consumption and prevent certain cancers. These advances in data and methods are fueling more opportunities for health economists to use state-of-the-art applied micro-econometric methods and credible research designs, including difference-in-difference, instrumental variables, regression discontinuity, and synthetic control methods, to evaluate the benefits of primary prevention of cancer interventions (98). Further, advances in data and methods have provided more opportunities for cancer health economists to 1) quantify the causal impacts of primary prevention of cancer to reduce common health conditions such as obesity, diabetes, and certain infectious diseases; 2) estimate the causal impacts of addressing socioeconomic, biological, and other factors that contribute to higher cancer rates in specific population groups; 3) leverage unconventional sources of data to identify and estimate the causal impacts of new primary cancer interventions deemed to reduce cancer risk; and 4) estimate the interactions of costs and cost-effectiveness of the impact of different environmental and occupational exposures on cancer risk based on where individuals were born, live, learn, work, and play (what is known as SDoH). The unconventional sources of data for health economics study may include cellular-based measures of consumer mobility. Additional opportunities involve public–private data partnerships, such as linking SEER and MarketScan data to study etiology and risk factors of cancer in individuals younger than 65 years who are members of specific populations. Further, in recent years, data scientists have developed variable selection methods, including least absolute shrinkage and selection operator (LASSO), regression trees, and random forests (97), which offer more opportunities for health economists to apply these new methods in studying primary prevention of cancer. Another opportunity for health economics research in primary prevention of cancer could be to use machine-learning (96) and big data methods (97) to estimate the causal impacts of novel preventive interventions. For example, recent studies have reported evidence that a substantial proportion of cancers are developed through chronic inflammation, which is linked to various steps involved in tumorigenesis (99–103). There may be multiple types of primary prevention opportunities to address chronic inflammation that can be identified using these advanced approaches as well as a corresponding need to assess their associated causal impacts. Another opportunity for health economics research is the need to incorporate the impacts of macroeconomic factors in primary prevention of cancer. Many of the modifiable risk factors discussed in this article (poor diet, physical inactivity, tobacco use, harmful alcohol consumption, and occupational and environmental exposures) have negative impacts on employment, national productivity, and health insurance coverage. A recent systematic review reported evidence of little attention devoted to macroeconomic impacts associated with noncommunicable disease, including cancer prevention (104). With advances in data science, health economists can use prevention impact models to estimate causal linkages of cancer risk factors, macroeconomic burden, and primary prevention of cancer. Future Directions for Enhancing Health Economics Research on Primary Prevention of Cancer The continued declines in annual cancer death rates in the past 2 decades are a strong indication of progress in cancer control (1), including the role of primary prevention. For example, many reports have credited tobacco prevention and control efforts as one of the major contributing factors to substantial decline in lung cancer (15,79,105). On the other hand, in recent years, we have observed rising incidence rates of some cancers associated with behavioral factors such as alcohol consumption, high sugar consumption leading to excess body weight, and physical inactivity (74,75,77). The rising incidence of these cancers makes a compelling case for improvements in prevention and in health economics research to quantify the outcomes of primary prevention of cancer interventions. Health economic outcomes may serve as an aid to raise awareness, guide recommendations for preventive action, prioritize resources, assist in policy development, and prepare models to monitor the long-term impacts of primary prevention of cancer. Economic decision models in particular serve these roles by acting as comprehensive evidence reviews that bring together disparate data sources to quantify the health and financial benefits and potential side effects of primary prevention. Based on the existing gaps, needs, challenges, and opportunities in health economics research in primary prevention of cancer, the following considerations are offered as potential next steps. First, because of the complex interactions of preventable factors causally associated with the development of cancer, health economics research has an integral role to play to quantify the costs and benefits of primary prevention of cancer interventions, programs, and policies. Building the economic evidence base contemporaneously with the evidence base on cancer risk factors and intervention effectiveness may speed appropriate adoption of primary prevention of cancer interventions. This effort would benefit from improvements in data modernization, training of the workforce, and methods related to health economics in basic and applied research. Second, it has been reported that the impacts of primary prevention of cancer interventions for most environmental and occupational exposures found to be convincing or probable evidence of carcinogens to humans have not been quantified (20,86). This gap could be addressed with multidisciplinary collaborative teams involving health economists, epidemiologists, toxicologists, and individuals from other disciplines to collect appropriate data and develop appropriate methods to quantify the health and economic benefits of interventions that can eliminate or decrease exposures to specific environmental and occupational carcinogens. Third, because of the COVID-19 pandemic, access to many preventive interventions such as tobacco cessation programs, healthy foods, and physical activity has been substantially reduced, and this may affect longer-term health outcomes (106). Health economists can use different economic methods to guide decisions on the health benefits of continued primary prevention of cancer interventions during or after a pandemic like COVID-19 or any other natural disaster. Finally, health economics researchers can apply existing methods or develop new ones to examine how health literacy may affect the efforts of primary prevention of cancer. This could be invaluable in generating new knowledge that can promote the optimal design of primary prevention of cancer interventions to populations that are medically underserved or populations that have been economically or socially marginalized. These and other forms of social inequities contribute to health disparities, which have been amplified during the COVID-19 pandemic (107,108). Related to this, cancer health economics researchers could use findings from their research to communicate broadly and in appropriate formats to community-based partners and relevant policy makers. Conclusions Health economics is a discipline with a unique role in quantitative evaluation of public health interventions. Specifically, the field has an important role in adding to the evidence used to evaluate the business case for primary prevention of cancer. This requires providing valid and credible information on the costs and benefits of a wide range of preventive measures, such as reducing tobacco use and consumption of foods low in nutritional value, controlling infectious virus and bacteria through vaccination and treatment, avoiding intensive sun exposure, decreasing sedentary behavior, reducing alcohol consumption, and reducing environmental and occupational exposures to carcinogenic agents. Maximizing the potential contribution of the field of health economics to primary cancer prevention can be supported by modernization of data systems, enhanced training of the health economics workforce, improvements in analytic methods, and increased opportunities for interdisciplinary collaboration. With time, these efforts can help to promote overall health in the short term and reduce cancer incidence and morbidity in the long term. Funding No funding was received for this commentary. Notes Role of the funder: Not applicable. Disclosures: The authors indicate no conflicts of interest. Author contributions: Conceptualization: DUE, MTH, DSK. Project administration: DUE. Visualization: DUE, MTH, DSK. Writing, original draft: DUE, MTH, DSK. Writing, review, and editing: DUE, MTH, DSK, HWC, MA, JD, YRH, MM, MFP. Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. Prior presentation: Some of this content was presented at the 2020 Future of Cancer Health Economics Research virtual conference. References 1 Islami F , Ward EM, Sung H, et al. Annual report to the nation on the status of cancer, part 1: national cancer statistics . 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JNCI MonographsOxford University Press

Published: Jul 5, 2022

References